BACKGROUND AND PURPOSE
Hemiparesis or hemiplegia, that is, the loss of some or all voluntary muscle activation on one side of the body, is a common impairment following stroke. The reduced ability to move leads to prolonged periods of time spent immobile.1-3 A major concern for rehabilitation clinicians is the time spent with the upper extremity resting in the lap. In this posture, shoulder and arm muscles, particularly shoulder internal rotators and extenders, and elbow flexors, are held in shortened positions, potentially leading to loss of available motion and contractures.4 To address this concern, people with hemiparesis or hemiplegia are often prescribed range-of-motion (ROM) exercises. Data supporting the effectiveness of ROM and stretching exercise in preventing loss of motion and contractures after stroke are inconclusive.4-7
A related concern for rehabilitation clinicians is whether or not performing ROM exercises contributes to hemiparetic shoulder pain.8,9 Hemiparetic shoulder pain is a disabling condition with many possible etiologies,10-12 affecting up to 72% of people with hemiparesis.11,13,14 ROM exercises could be one factor contributing to shoulder pain secondary to altered scapular and humeral movement patterns. Precise scapulohumeral coupling is needed to preserve the suprahumeral space and prevent impingement of the rotator cuff tendons. Proper coupling includes upward rotation and posterior tilting of the scapula15-18 and external rotation of the humerus.15,16 Reduced voluntary neural drive due to the stroke may disrupt the timing and activation of scapulothoracic and rotator cuff muscles.19 When assistance is provided to move the arm during an exercise, the humerus may be pushed into elevation angles higher than those that the person can actively produce without assistance. When prescribing ROM exercise to preserve movement and avoid contractures, care must be taken to avoid exercises that could contribute to the development or persistence of hemiparetic shoulder pain.
The purpose of this study was to examine the scapular and humeral movement patterns in people with hemiparesis poststroke when performing commonly prescribed ROM exercises: person-assisted ROM, self-assisted ROM, and cane-assisted ROM. The scapular and humeral movement patterns during the exercises in participants with stroke were compared with those of a group of neurologically intact healthy control subjects performing scapular plane shoulder elevation, which was our best proxy for normal shoulder motion. We hypothesized that people with hemiparesis would have abnormal scapular and humeral movement patterns when performing the selected exercises. In addition, we hypothesized that the extent of movement abnormality would be related to the severity of reported pain during that movement. A better understanding of the scapular and humeral movement patterns associated with commonly prescribed ROM exercises may help clinicians identify which exercises are to be avoided and how exercises may be modified to better replicate the scapular and humeral movement patterns of normal shoulder motion.
This was a pilot sample of convenience. Thirteen subjects with hemiparesis were recruited from a local rehabilitation hospital. Subjects with hemiparesis were included if they had (1) a diagnosis of stroke and (2) unilateral upper extremity weakness following stroke. Subjects were excluded if they (1) had a history of shoulder pain and pathology prior to stroke, (2) were unable to follow 2-step commands, (3) showed signs of hemineglect, (4) showed pain symptoms consistent with referral from the cervical or thoracic spine, (5) had any serious medical complications that would prevent them from participating, and/or (6) were unable to provide informed consent.
Twelve healthy subjects were recruited from the community. The age and gender composition of the control group was selected to match the age and gender composition of the hemiparetic group. Control subjects were excluded if they (1) had a history of stroke, (2) had history or current complaints of shoulder pain or history of diagnosed shoulder pathology, (3) had any serious medical conditions that would prevent them from participating, and/or (4) failed to provide informed consent. The study was approved by the Human Research Protection Office of Washington University in St. Louis prior to recruitment and testing. All subjects signed informed consent documents before participating.
Computer-based kinematic techniques were used to quantify movement of the contralesional, more-involved shoulder, arm, and thorax.20 Three-dimensional movements of the upper extremity were captured using an electromagnetic tracking system (Motion Monitor built around Flock of Birds, Innovative Sports Training Inc, Chicago, Illinois). Four sensors were attached to the (1) trunk (mid-sternum), (2) the arm (proximal to the lateral epicondyle, bisecting the arm mass), (3) the forearm (proximal to the midpoint between the radial and ulnar styloids on the dorsum of the forearm), and (4) the scapula (distal flat aspect of the acromion) (Figure 1).21 The forearm sensor was initially included to monitor whether subjects were moving with a flexed elbow; since this did not occur, elbow sensor data are not included in this report. All sensors and trailing wires were secured with tape and Coban (3M, St Paul, Minnesota) to prevent slippage and arbitrary sensor movement. The hardware manufacturer reports a root-mean-square accuracy of 0.5° for orientation and 1.8 mm for position for the sensors used. With arms relaxed, bony landmarks on the thorax, scapula, and humerus were digitized with a custom probe to permit transformation of sensor data into local segment coordinates, using the accepted order of internal/external rotation, upward/downward rotation, and posterior/anterior tilting, according to the protocol recommended by the International Society of Biomechanics, Shoulder Group.20 Glenohumeral joint center was estimated using a least-squares algorithm to find the point on the humerus that moved least in respect to the scapula as it was moved through short arcs.
Kinematic data were low-pass filtered at 6 Hz by using a second-order Butterworth filter. Motion Monitor software was used to calculate and extract segmental position and angle data from the sensor data using standard rigid body methodology.20 The scapulothoracic angular data extracted were scapular upward rotation and scapular tilt, and the glenohumeral angular data were humeral elevation and humeral external rotation (Figure 2). Scapular internal/external rotation data were also extracted but are not included in this report because of lack of consensus regarding what constitutes normal scapular internal and external rotation during humeral elevation with some studies reporting scapular external rotation as the arm is elevated18,22,23 and some studies demonstrating scapular internal rotation as the arm is elevated.24-26 Anatomical variations in the shape and size of the thorax and ribs could also impact the relative internal and external rotation of the scapula as it slides along the thorax. The plane of elevation for humeral elevation depended on the exercise, but generally this elevation occurred between the sagital plane and the scapular plane (approximately 30° anterior to the frontal plane by visual estimation). Scapular upward rotation was rotation of the scapula in frontal plane about an anterior-posterior axis in which the inferior angle moves laterally. Scapular posterior tilt was rotation of the scapula in the sagital plane about a lateral axis in which the superior border of the scapula moves posteriorly. Humeral external rotation was the spinning of the humerus on the glenoid laterally. All angular data were calculated according to the recommended protocol.20 For ease of communication, humeral external rotation data were multiplied by −1. Custom-written software in MATLAB (The Mathworks Inc, Natick, Massachusetts) was used for subsequent analysis to find the angles mentioned earlier at the start of movement (0°) and at 30°, 60°, 90°, and 120° of humeral elevation.
Testing began with subjects seated in a wooden chair with the upper limb hanging freely. Care was taken to ensure that the tested upper extremity and scapula neither contacted nor were otherwise obstructed by the chair. Subjects performed 3 trials of each exercise at a self-selected pace and were given rest breaks as needed. All subjects were able to perform the exercise as instructed, although some required several practice trials to perform the movement correctly before trials were recorded. Control subjects were tested using the same self-selected speed protocol as subjects. A single examiner performed all the testing and digitizing.
The 3 commonly prescribed ROM exercises were person-assisted ROM, self-assisted ROM, and cane-assisted ROM (Figure 3). All exercises were performed as active-assisted ROM, in that the subjects used their more-involved extremity as much as possible, and the assistance provided additional ROM beyond what they could do unassisted. Person-assisted ROM (Figure 3A) was performed by a single tester. Assistance was given by another person via hand contact under the middle portion of the arm and under the mid-forearm as the subject performed humeral elevation.7 Self-assisted ROM (Figure 3B) was performed with subjects supporting the elbow of the more-involved extremity with the less-involved extremity as they performed humeral elevation.6 Person-assisted and self-assisted ROM occurred near the plane of flexion. Cane-assisted ROM (Figure 3C) was performed using a plastic pipe that approximated the diameter and length of a standard cane. Subjects gripped the cane with an overhand grip with hands slightly wider than shoulder width apart. They performed bilateral shoulder elevation, providing assistance from the less-involved extremity through the cane to assist the more-involved extremity. Cane-assisted ROM occurred in the scapular plane. As is done in the clinical setting, the examiner provided assistance with grasping the cane if needed. All subjects could produce at least minimal forces to grip the cane once they had grasped the cane.
All exercises were compared to scapular plane shoulder elevation as performed by control subjects because this represents the best proxy for normal scapular and humeral motion, and it is often used to examine shoulder motion in healthy control subjects and patient populations.18,21,23,27,28 We did not compare scapular and humeral movements of the more-involved shoulder with those of the less-involved shoulder because the less-involved shoulder has been found to have kinematic alterations29 and was assisting with 2 of the 3 exercises. Comparisons were not made to control subjects performing the exercises because that would be a contrived situation; that is, people with healthy shoulders would not perform these exercises.
Shoulder pain at rest and during movement trials was recorded using a numeric pain rating scale (0-10 points). Subjects rated their pain before testing and after each trial. This scale has been shown to be a reliable and sensitive pain scale for use in older populations.30 It has good reliability in subjects with orthopedic shoulder conditions31 as well as subjects with hemiparesis.32 The Stroke Impact Scale, Hand Function subscale was used to capture upper extremity functional deficits.33 This reliable, valid, and quick measure agrees well with the more time-consuming Fugl-Meyer Upper Extremity Motor subscale.34 Muscle tone at the elbow and shoulder was assessed using the Modified Ashworth Scale.35
Statistica (StatSoft Inc, Tulsa, Oklahoma) was used for statistical analyses and the criterion for statistical significance was set at P < 0.05. A repeated-measures ANOVA and post hoc t tests were used to compare pain at rest (before performing any movement) and pain during exercise (quantified by the average numeric postexercise pain rating during the 3 trials). Mixed-model, repeated-measures ANOVAs were used to test for significant differences in humeral external rotation, scapular upward rotation, and scapular tilt between the hemiparetic group performing each exercise and the control group performing scapular plane shoulder elevation at the start of movement (0°), 30°, 60°, and 90° of humeral elevation. For each exercise, the average of the 3 trials for each subject was entered into the ANOVAs. Because we used a single control condition (control group scapular plane shoulder elevation), we ran separate ANOVAs for each exercise versus the control condition. Post hoc comparisons using the Fisher Least Significant Difference were used when significant main or interaction effects were found. Protected t tests with a more stringent criterion of P < 0.01 were used to assess differences at 120° since many hemiparetic subjects did not achieve this angle. This analysis strategy permitted the inclusion of all subjects in the ANOVAs yet still examined the higher humeral elevation angles.
Since some of our subjects had shoulder pain and others did not, we used Spearman ρ correlations to test whether severity of pain during performance of each specific exercise was related to scapular and humeral movement at various humeral angles during that same exercise. This would provide an indication as to how pain may have influenced the recorded movements.
Characteristics of the 13 subjects with hemiparesis and characteristics of 12 control subjects are provided in the Table. Time since stroke for the hemiparetic subjects was variable, ranging from 1 month to 2 years. As expected, upper extremity function was decreased and average spasticity levels were mild, as indicated by the Hand Function subscale of the Stroke Impact Scale and the Modified Ashworth Scale, respectively.
Five hemiparetic subjects reported pain in their involved shoulder before testing. Of the eight hemiparetic subjects who did not report pain before testing, four experienced some shoulder pain during various exercises. On average, the hemiparetic group reported mild pain at rest, which increased during performance of the exercises (bottom of the Table). Pain was increased during the performance of the exercises compared to rest (within-subjects main effect, F3,36 = 4.01, P = 0.015). Post hoc t tests indicated that pain during the performance of person-assisted ROM and self-assisted ROM were greater than pain at rest (P = 0.03 and P = 0.02, respectively), and pain during the performance of cane-assisted ROM showed a trend toward greater pain than did pain at rest but did not reach significance (P = 0.08).
Scapular and Humeral Movement During the 3 Exercises
Scapular and humeral movement data from the 3 exercises in the hemiparetic group and from scapular plane shoulder elevation in the control group are shown in Figure 4. Here we report the relevant main effects of group and group × angle interactions as they pertain to our hypotheses. For the post hoc testing of group × angle interactions, we indicate the comparisons where significant differences were not found. As expected, there were main effects of angle for each exercise across the examined motions (P < 0.05).
In the person-assisted ROM exercise (Figure 4, top row), the hemiparetic group had decreased humeral external rotation (main effect of group, F1,23 = 14.2, P < 0.001; group × angle interaction, F3,72 = 10.2, P < 0.001; post hoc testing yielded no significant difference at 0°, P = 0.30) and decreased scapular upward rotation (main effect of group, F1,23 = 4.4, P < 0.05; group × angle interaction, F3,72 = 4.5, P < 0.006; post hoc testing yielded no significant difference at 0°, P = 0.70) compared to control subjects performing scapular plane shoulder elevation. Protected t tests at 120° demonstrated decreased humeral external rotation (P < 0.01), but no difference in scapular upward rotation (P = 0.42) in the hemiparetic group compared with the control group. Scapular tilt was not different between groups (main effect of group, F1,23 = 1.1, P = 0.32; at 120° protected t test, P = 0.44).
In the self-assisted ROM exercise (Figure 4, middle row), the hemiparetic group had decreased humeral external rotation (main effect of group, F1,23 = 29.4, P < 0.001; group × angle interaction, F3,72 = 19.3, P < 0.001; post hoc testing yielded no significant difference at 0°, P = 0.86) compared with control subjects performing scapular plane shoulder elevation. Protected t tests at 120° demonstrated decreased humeral external rotation (P < 0.001) in the hemiparetic group compared with the control group. Scapular upward rotation was not different between groups (main effect of group, F1,23 = 1.9, P = 0.18) but showed a group × angle interaction (F3,72 = 5.1, P <0.003; post hoc testing yielded no significant difference at 0°, P = 0.90). Scapular upward rotation was not different at 120° (protected t test, P = 0.57). Scapular tilt was not different between groups (main effect of group, F1,23 = 0.5, P = 0.49; at 120° protected t test, P = 0.75).
In the cane-assisted ROM exercise (Figure 4, bottom row), the hemiparetic group had decreased humeral external rotation (main effect of group, F1,23 = 15.5, P < 0.001; group × angle interaction, F3,72 = 15.9, P < 0.001; post hoc testing yielded no significant difference at 0°, P = 0.31) compared with control subjects performing scapular plane shoulder elevation. Protected t tests at 120° demonstrated decreased humeral external rotation (P < 0.001) in the hemiparetic group compared with the control group. No differences between groups were found for scapular upward rotation (main effect of group, F1,23 < 0.01, P = 0.95; at 120° protected t test P = 0.65) or scapular tilt (main effect of group, F1,23 = 1.6, P = 0.22; at 120° protected t test P = 0.73).
Relationships Between Pain and Movement
No relationships were found between reported pain during the performance of each exercise and the scapular and humeral movement data. Spearman ρ values ranged from −0.46 to +0.36 (all Ps > 0.05).
The results of our study indicate that the hemiparetic group had altered movement patterns during performance of the ROM exercises compared to our proxy of normal shoulder motion. On average, the subjects with hemiparesis had mild pain at rest, which increased during the performance of the exercises. Severity of pain was not related to the extent of abnormality in the scapular or humeral movement patterns during the exercises.
Our primary hypothesis was supported: people with hemiparesis had abnormal scapular and humeral movement patterns when performing the tested exercises. The performance of stretching and ROM exercises has been previously reported to be associated with shoulder pain in people with hemiparesis.8,9 Our data build on these reports by describing abnormal scapular and humeral movements that occurred during the performance of shoulder ROM exercises. Data from the present study provide a biomechanical mechanism for how performing these exercises may contribute to the development of shoulder pain poststroke.
The most salient finding during the performance of all 3 exercises was the decrease in humeral external rotation. The lack of dynamic humeral external rotation found in the present study is consistent with literature showing an association between reduced passive humeral external rotation and hemiparetic shoulder pain.32,36-38 Conditions that decrease humeral external rotation increase rotator cuff compression, particularly compression against the greater tuberosity; the compression increases as the humerus is elevated.39-41 We speculate that performing these ROM exercises as described could contribute to, or exacerbate, hemiparetic shoulder pain by repeatedly compressing the rotator cuff tendons.
It is worth noting that the etiology and contributing factors of shoulder pain following stroke are multifactorial and poorly understood.11,12,36,42-44 It is likely that more than 1 factor is responsible. These factors may overlap extensively and no single factor may be responsible for pain in individual patients. These factors include shoulder subluxation, reflex sympathetic dystrophy, and adhesive capsulitis. The resultant disruptions in movement patterns, regardless of diagnosis, can lead to strain and tearing of rotator cuff muscles as well as impingement of the rotator cuff tendons. It appears that performing ROM exercises as described may be promoting these abnormal movement patterns and thus should be modified or avoided in this population.
Our secondary hypothesis was not supported: the extent of movement abnormalities was not related to the extent of pain during the selected exercise. There are 3 possible explanations for this finding. First, it is possible that severity of pain is not related to the extent of movement abnormalities as seen in this sample. This possibility is consistent with the understanding that the experience of pain is influenced by many factors.45-47 The extent of scapular and humeral movement abnormalities might therefore be only one of many contributing factors. Alternatively, it is possible that the relationship between pain and extent of movement abnormalities is affected by time; that is, performing many repetitions of these exercises over a long period would create an association between pain severity and abnormal movement. In this alternative scenario, the effects of rotator cuff compression incurred while performing these exercises would accumulate. The eventual result might be microtrauma and pain, which in turn could lead to more abnormal movement patterns.48 Since we did not investigate other factors that may have contributed to the reported pain, and we tested only 3 repetitions of each exercise, our data do not permit us to distinguish between these possibilities. A third possible reason for the lack of relationship is the small sample size of this study (see suggestions for future studies under the “Limitations” section given later).
Clinical Considerations for When Prescribing Specific Exercises Poststroke
Of the 3 exercises evaluated, person-assisted ROM of the hemiparetic shoulder had the most differences in scapular and humeral motion compared with active ROM of the normal shoulder. These differences, decreased humeral external rotation and scapular upward rotation, may be attributed to the fact that the scapula and humerus were not monitored or controlled during performance of this exercise. A skilled therapist performing this same exercise may be much more likely to monitor and control these motions. It is often the case, however, that a therapist provides the initial instruction, and then this exercise is performed repeatedly with assistance from a nonskilled caregiver. We sought to replicate this common method of performance. The results of this study, therefore, highlight the importance of education to caregivers who may be performing this person-assisted ROM exercise on people with hemiparesis. Specific education about how to externally rotate the humerus and manually assist the scapula into upward rotation may be needed to perform this exercise with more normal shoulder motions.
The self-assisted ROM exercise resulted in decreased humeral external rotation compared with normal shoulder motion. Using the less-involved upper extremity to assist their more-involved upper extremity naturally places both arms into horizontal adduction and internal rotation; this is particularly true for larger individuals with wide trunks. On the basis of these mechanical constraints, therapists may want to avoid the self-assisted ROM exercise when considering options to preserve movement and prevent contractures in people with hemiparesis poststroke.
The cane-assisted ROM exercise also resulted in decreased humeral external rotation compared with normal shoulder motion. An overhand grip was used to grip the cane in the present study. The overhand grip placed the forearm in pronation and likely contributed to a less externally rotated humerus. One way to modify this exercise would be to switch to an underhand grip. The underhand grip would position the forearm in supination and may help to promote humeral external rotation. A challenge to making this modification is that people with stroke may have more trouble maintaining an underhand grip with the paretic hand compared with an overhand grip. This could be addressed with a strap or other individualized modification. We speculate that, if modified to employ an underhand grip, the cane-assisted ROM exercise may be an acceptable choice for preserving shoulder movement and preventing contractures in people with hemiparesis poststroke. It should be noted, however, that at this time the clinical premise that contractures can be prevented through ROM exercises is not fully supported by data.49
Three main limitations should be taken into account when interpreting the results of this study. First, the sample size was small, limiting the ability to detect differences between groups, to identify relationships to pain, and to generalize our findings. Second, we studied only 3 ROM exercises, each performed according to specific instructions. Other exercises and their variations may have different effects on the movement patterns of the humerus and scapula. Finally, our sample included people with hemiparesis both with and without shoulder pain. While people with and without pain are prescribed ROM exercises during their rehabilitation, grouping them together could have masked findings unique to one subgroup or the other. Future longitudinal studies on this topic with larger sample sizes, more variations of exercises, and grouping of subjects into subpopulations with respect to pain would greatly improve the therapist's decision making when choosing exercises for people with poststroke hemiparesis.
Reduced humeral external rotation was the most common movement abnormality observed during the performance of 3 commonly prescribed shoulder ROM exercises by people with hemiparesis poststroke. Results were different depending on whether exercise performance was person-assisted, self-assisted, or cane-assisted. There appears to be little relationship between the severity of pain experienced with exercise and the extent of movement abnormality. Our data can assist clinicians in making decisions regarding which ROM exercises to prescribe to preserve shoulder motion and prevent contractures in this population.
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kinematics; rehabilitation; shoulder pain; stroke