Volume 88, Issue 8 , Pages 1016-1021, August 2007
Predictability of Simple Clinical Tests to Identify Shoulder Pain After Stroke
Article Outline
Abstract
Rajaratnam BS, Venketasubramanian N, Kumar PV, Goh JC, Chan Y-H. Predictability of simple clinical tests to identify shoulder pain after stroke.
Objective
To identify simple diagnostic musculoskeletal tests that can be performed early after stroke to predict patients’ likelihood of reporting early signs of hemiplegic shoulder pain.
Design
Case control.
Setting
Multicenter acute care hospitals.
Participants
A total of 152 adults after a first episode of stroke, of whom 135 met the inclusion criteria. Thirty patients were assigned to the experimental group because they reported moderate intensity of hemiplegic shoulder pain at rest. The remaining 105 patients made up the control group.
Interventions
Not applicable.
Main Outcome Measures
Therapists measured the performance of combined upper-limb movement including the hand-behind-neck (HBN) maneuver, passive pain-free ranges of shoulder motion, 3 musculoskeletal tests, and the strength of deltoid muscles during each patient’s hospital stay. The numeric rating scale (NRS) identified those who reported moderate or greater intensities of hemiplegic shoulder pain during rest and during assessment.
Results
In our study, 22.2% (95% confidence interval, 15.5−30.2) of the patients reported hemiplegic shoulder pain, on average 1 week after the onset of stroke. Positive Neer test (NRS score ≥5) during the HBN maneuver and a difference of more than 10° of passive range of external rotation between shoulders had a 98% probability of predicting the presence of hemiplegic shoulder pain (receiver operating characteristic, .994; sensitivity, 96.7%; specificity, 99.0%; positive predictive value, 96.7%; negative predictive value, 99.0%; P<.001).
Conclusions
Three diagnostic clinical tests that can be performed during a bedside evaluation increase the likelihood of determining those who complain of hemiplegic shoulder pain after an acute episode of stroke.
Key Words: Hemiplegia, Musculoskeletal system, Pain, Rehabilitation, Shoulder pain
HEMIPLEGIC SHOULDER PAIN is among the 4 most common, yet preventable, medical complications that patients may experience after stroke.1, 2, 3, 4, 5 It can commence as early as the first 2 weeks after stroke.1, 3, 4, 5, 6, 7 Seventeen percent of patients experienced shoulder pain within the first week,3 55% within 2 weeks,4 87% by 2 months,4 and 75% within the first year after stroke.8, 9, 10 The early onset of hemiplegic shoulder pain adversely hindered the recovery of upper-limb function because it has been reported that improvement in upper-limb function within the first 5 weeks poststroke translated to greater usage of the affected limb during performance of functional tasks.11
Musculoskeletal conditions of noncentral origin such as glenohumeral instability, rotator cuff tears, subacromial and supraspinatus impingement, shoulder-hand syndrome, biceps tendonitis, and shoulder muscle atrophy also occurred after stroke.7, 8, 12, 13, 14, 15, 16, 17 Less than 2 months after stroke, arthroscopic evaluations by Lo et al13 identified 11 different types of shoulder pain etiology. Fifty percent of patients experienced adhesive capsulitis13 and the incidence rose to 74% within a year.18 Restriction in shoulder external rotation also occurred among patients with severe shoulder pain less than 3 months after stroke.18, 19, 20 Some authors attributed the early limitation in shoulder ranges of motion (ROMs) to soft tissue contractures13 because patients with hemiplegic shoulder pain showed synovial hypervascularization and cellular proliferation without inflammatory infiltration.21 Other histologic findings among patients with adhesive capsulitis and shoulder-hand syndrome included elevated growth factor β, fibroblasts, tumor necrosis factor α, and infiltration of perivascular leukocytes into the capsule.22, 23 Capsular adhesions further limited passive shoulder external rotation.23, 24
During the early phase of recovery, 65% of patients also experienced muscle weakness with no or minimal degenerative changes within the glenohumeral joint.4 Patients with both low muscle tone and hemiplegic shoulder pain were at a greater risk of experiencing glenohumeral instability and impingement syndromes.7, 14, 22, 25, 26 Glenohumeral instability and subacromial impingement are commonly diagnosed by simple and noninvasive apprehension, Neer, and sulcus tests,27 but these tests are not usually performed on patients early after the onset of their stroke. Furthermore, there is a lack of reliable diagnostic clinical tests to identify the exact musculoskeletal etiologies associated with hemiplegic shoulder pain.
The purpose of this study was to explore the association between early reporting of hemiplegic shoulder pain among patients who experienced an acute episode of stroke with differences in their shoulder ROMs, muscle strengths, muscle tones, and positive findings of musculoskeletal clinical tests to predict the likelihood of underlying shoulder dysfunction. The secondary aim of the study was to establish valid and simple diagnostic clinical tests that could predict those patients at risk of developing hemiplegic shoulder pain.
Methods
Design
The institutional review boards of 3 general hospitals approved this multicenter study that was conducted between October 2002 and May 2003.
Participants
Physical therapists from the hospitals recruited 152 adult inpatients who had experienced a first episode of acute stroke. Stroke was diagnosed as a focal disturbance of cerebral function due to vascular origin lasting more than 24 hours. Patients were included in the study if they were medically stable, cognitively oriented, and able to verbally express their needs. The exclusion criteria were bilateral stroke, thalamic infarcts, upper-limb sensory deficit, previous shoulder injury or pathology, reflex sympathetic dystrophy, receptive dysphasia, or unstable angina. The cuff tightness test described by Price et al28 confirmed that patients had the ability to differentiate levels of pain intensities. Seventeen patients were rejected because they showed mild alterations in their arm sensation or had early signs of shoulder-hand syndrome. One hundred thirty-five patients provided informed consent before they participated in the study.
Measurements
The definition of shoulder pain was in accordance with the Arthritis and Rheumatism Council Epidemiological Research Unit criteria of an expression of continuous pain.29 The 11-point numeric rating scale (NRS) quantified the intensity of pain, with 10 being the most intense level of pain and 0 being no pain. The NRS is a valid and sensitive graded pain intensity scale that is simple to use and highly recommended for studies involving older patients.30 In the present study, 30 patients reported moderate and greater (NRS score ≥5) intensities of shoulder pain at rest during their hospital stay. They were the experimental group, referred to as hemiplegic shoulder pain in the present study. The rest of the recruited patients (controls) reported mild or no shoulder pain at rest.
Physical therapists conducted all clinical tests at the patients’ bedside or during rehabilitation sessions within their hospital stay (mean, 8.62±6.6d). These tests included the following.
Clinical examination of shoulder ROMs and muscle strengthsA goniometer was used to quantify the pain-free ranges of passive flexion, passive extension, passive abduction, and passive external rotation of all patients. Measurements were taken while patients were supine or side-lying and in accordance with the established protocol. ROMs were compared with the unaffected upper limb and the differences expressed as a percentage of the available range of the unaffected upper limb in a particular direction. Passive ROM of all shoulder motions was divided into 2 categorical variables, that is, 10° of difference or less and more than 10° of difference.
The ordinal scale of the manual muscle test quantified muscle strength of the anterior, middle, and posterior fibers of the deltoid muscles. The scale reported a good to very good interrater (weighted κ range, .85−.94) and intrarater (weighted κ range, .81−.96) agreements when performed on patients who experienced an acute episode of stroke.31, 32 The muscle strength of the deltoids were categorized into less than gravity, and equal to or greater than gravity. To keep the assessment simple and quick to perform, the strength of other shoulder muscles was not tested.
The Modified Ashworth Scale (MAS) quantified upper-limb muscle tone, because the scale has been reported to have good to very good interrater (weighted κ range, .77−.96) and intrarater (weighted κ range, .77−.83) agreements among patients who experienced stroke.32, 33 Muscle tone of the upper limb was categorized as normal when the MAS score was 0 to 1+ and high when the score was 2 to 4. Low tone reflected a flaccid upper limb.
Combined upper-limb movementsThe performance of dorsum of hand to lumbosacral junction (hand-behind-back [HBB]) maneuver reflects the combination of shoulder internal rotation and extension, whereas hand-behind-neck (HBN) maneuver is a combination of shoulder external rotation and abduction.34 The therapist placed each patient’s affected arm passively in both positions, one at a time, while patients reported the intensity of shoulder pain they experienced.
Musculoskeletal testsTherapists performed the apprehension, Neer, and sulcus tests on the affected upper limb of all patients. The apprehension test is performed by placing the patient in supine position with their arm externally rotated, in abduction and slight extension. Reporting of shoulder pain or signs of apprehension during the test suggest the likelihood that the patient may have signs of anterior shoulder instability (sensitivity, 63%).27, 35, 36, 37 In the sitting position, the therapist performed the Neer test by limiting each patient’s scapular rotation while internally rotating the affected arm in a passive mode through elevation in the scaphoid plane.27, 38 Shoulder pain during this test is suggestive of subacromial impingement.27, 35, 36, 38 The Neer test has a sensitivity of 88.7%.35, 36, 38, 39, 40, 41 The sulcus test was performed in the sitting position with patient’s affected arm by their side while the therapist pulled the elbow inferiorly to measure the physiologic separation between the acromial and the humeral head. Separation of less than 1cm is scored as 1, 1 to 2cm is scored as 2, and greater than 2cm is scored as 3. A grade 3 sulcus test indicates likely etiology of multidirectional glenohumeral instability. The test has a sensitivity of 28%.27, 35, 36
Reliability Phase
A reliability study evaluated the agreement of recording of hemiplegic shoulder pain, HBB maneuver, HBN maneuver, posterior deltoid strength, and passive external rotation performed on 17 patients by 2 physical therapists. The second physical therapist was unaware of the results of the first therapist and revisited all 17 patients at least 2 hours after the completion of the initial examination. There was a high degree of reliability between the 2 therapists (table 1).
Table 1. Interrater Reliability of Selected Clinical Tests
| Clinical Tests | ICC | 95% CI | |
|---|---|---|---|
| Lower Bound | Upper Bound | ||
| Complaint of hemiplegic shoulder pain at rest | .969 | .918 | .989 |
| HBN maneuver | .979 | .934 | .993 |
| HBB maneuver | .979 | .942 | .992 |
| Difference in passive ROM of external rotation | .916 | .786 | .968 |
| Strength of posterior deltoid | .979 | .944 | .992 |
Statistical Analysis
Reports indicated that approximately 20% of patients experienced hemiplegic shoulder pain during their hospital stay.3, 17, 24 Thus, the minimum sample size required was identified to be 132 patients at a 95% confidence interval (CI) (15−25). SPSSa for Windows facilitated statistical analysis. During the reliability phase of this study, intraclass correlation coefficient (ICC) at 95% CI was calculated. Parametric t tests determined mean differences between the hemiplegic shoulder pain and controls. Chi-square tests evaluated the association between patients with hemiplegic shoulder pain and the categorical variables. Clinical measures of HBN maneuver, HBB maneuver, passive shoulder ROMs, and muscle strengths were categorized to obtain receiver operating characteristic (ROC) values from binary logistic regression analyses. The full predictive clinical model consisted of the highest significant ROC value for each clinical test. This study also reported sensitivity, specificity, positive predictive value (PPV), negative predictive value (NPV), positive and negative diagnostic likelihood ratios (LR+, LR−), respectively, and probability of all clinical tests and variables. Significance level of all tests was P less than .05.
Results
Differences and Associations of Hemiplegic Shoulder Pain
Table 2 summarizes the characteristics and stroke status of all 135 patients. Most patients (83%) were aged over 55 years with a mean age of 64.36±10.82 years. Exactly 81.5% experienced an infarction that led to a stroke, which was consistent with the established epidemiologic health trends of the local population.42 In our study, 22.2% (95% CI, 15.5−30.2) of patients reported hemiplegic shoulder pain at rest (NRS score ≥5). There was no association between hemiplegic shoulder pain at rest with age, sex, type of stroke, side of stroke, or muscle tone (P>.05). All clinical examinations of shoulder ROMs and shoulder muscle strengths differed statistically between hemiplegic shoulder pain and control patients (P<.001). Hemiplegic shoulder pain at rest was associated with lesser deltoid muscle strengths (P<.001) and greater than 10° differences in passive flexion (P=.001), passive abduction (P<.001), and passive external rotation (P<.001). However, there was no association between hemiplegic shoulder pain and passive ROM extension (P=.275).
Table 2. Characteristics, Stroke Status, and Clinical Examinations
| Variables | Controls (n=105) | Hemiplegic Shoulder Pain (n=30) | P |
|---|---|---|---|
| Mean age ± SD (y) | 64.36±10.8 | .256 | |
| Age distribution (y) | |||
| 34.3 | 46.7 | ||
| 35.2 | 20.0 | ||
| 30.5 | 33.3 | ||
| Sex | .417 | ||
| 54.3 | 50.0 | ||
| 45.7 | 50.0 | ||
| Type of stroke | .300 | ||
| 17.2 | 23.3 | ||
| 82.8 | 76.7 | ||
| Side of stroke | .138 | ||
| 60.0 | 46.7 | ||
| 40.0 | 53.3 | ||
| Upper-limb muscle tone | .056 | ||
| 69.5 | 56.7 | ||
| 16.2 | 10.0 | ||
| 14.3 | 33.3 | ||
| Anterior deltoid strength | <.001⁎ | ||
| 31.4 | 93.3 | ||
| 68.6 | 6.7 | ||
| Middle deltoid strength | <.001⁎ | ||
| 34.3 | 93.3 | ||
| 65.7 | 6.7 | ||
| Posterior deltoid strength | <.001⁎ | ||
| 47.6 | 96.7 | ||
| 52.4 | 3.3 | ||
| Passive ROM flexion | .001⁎ | ||
| 83.8 | 40.0 | ||
| 16.2 | 60.0 | ||
| Passive ROM extension | .275 | ||
| 53.3 | 6.7 | ||
| 46.7 | 93.3 | ||
| Passive abduction | <.001⁎ | ||
| 90.5 | 53.3 | ||
| 9.5 | 46.7 | ||
| Passive external rotation | <.001⁎ | ||
| 82.9 | 6.7 | ||
| 17.1 | 93.3 | ||
⁎Significant at P<.001. |
Predictive Clinical Tests of Hemiplegic Shoulder Pain
Table 3 shows diagnostic properties of individual clinical tests and their cutoff based on the highest ROC values (P<.05). The complete predictive model consisted of positive apprehension and Neer tests, HBN score of 5 or greater, HBB score of 5 or greater, passive flexion difference of more than 5°, passive extension difference of more than 20°, passive abduction difference of more than 5°, passive external rotation difference of more than 10°, and the muscle strength in the 3 deltoid muscles of less than gravity. The ROC of the complete model of 11 clinical tests was .999 and the ROC remained unchanged when the predictive model consisted of only 6 clinical tests (table 4, model A). The ROC values of predictive models B and C consisting of 4 and 3 clinical tests, respectively, were slightly less. However, their sensitivity, specificity, PPV, NPV, LR+, and LR− were the same as model A. Model D versions I through III were combinations of 2 clinical tests each and reported smaller ROC values compared with model C. Although model C required only 3 clinical tests, when all 3 tests were positive there was a 98% probability of identifying complaints of hemiplegic shoulder pain at rest (table 5).
Table 3. Diagnostic Properties of Significant Clinical Tests Among Patients Who Complained of Hemiplegic Shoulder Pain at Rest (n=30)
| Tests | ROC | Sensitivity | Specificity | PPV | NPV | LR+ | LR− | P |
|---|---|---|---|---|---|---|---|---|
| Apprehension test (+ve) | .695 | 80.0 | 59.0 | 35.8 | 91.2 | 2.0 | 3.0 | .001 |
| Neer test (+ve) | .881 | 100.0 | 76.2 | 54.5 | 100.0 | 4.2 | ∞ | <.001 |
| HBN maneuver (NRS) | ||||||||
| .648 | 100.0 | 29.5 | 28.8 | 100.0 | 1.4 | ∞ | .014 | |
| .848 | 100.0 | 69.5 | 48.4 | 100.0 | 3.3 | ∞ | <.001 | |
| .848 | 100.0 | 69.5 | 48.4 | 100.0 | 3.3 | ∞ | <.001 | |
| .979 | 96.7 | 99.0 | 96.7 | 99.0 | 96.7 | 30.0 | <.001 | |
| .783 | 56.7 | 100.0 | 100.0 | 89.0 | ∞ | 2.3 | <.001 | |
| .683 | 36.7 | 100.0 | 100.0 | 84.7 | ∞ | 1.6 | .002 | |
| HBB maneuver (NRS) | ||||||||
| .652 | 100.0 | 30.5 | 29.1 | 100.0 | 1.4 | ∞ | .011 | |
| .738 | 100.0 | 47.6 | 35.3 | 100.0 | 1.9 | ∞ | <.001 | |
| .845 | 96.7 | 72.4 | 50.0 | 98.7 | 3.5 | 21.9 | <.001 | |
| .748 | 66.7 | 82.9 | 52.6 | 89.7 | 3.9 | 2.5 | <.001 | |
| .767 | 53.31 | 100.0 | 100.0 | 88.2 | ∞ | 2.1 | <.001 | |
| .700 | 16.7 | 100.0 | 100.0 | 80.8 | ∞ | 1.2 | .001 | |
| Passive flexion | ||||||||
| .781 | 93.3 | 62.9 | 41.8 | 97.1 | 2.5 | 9.4 | <.001 | |
| .719 | 60.0 | 83.8 | 51.4 | 88.0 | 3.7 | 2.1 | <.001 | |
| Passive extension | ||||||||
| .705 | 93.3 | 47.6 | 33.7 | 96.2 | 1.8 | 7.1 | .001 | |
| .733 | 93.3 | 53.3 | 36.4 | 96.6 | 2.0 | 8.0 | <.001 | |
| .762 | 93.3 | 59.0 | 39.4 | 96.9 | 2.3 | 8.8 | <.001 | |
| .781 | 93.3 | 62.9 | 41.8 | 97.1 | 2.5 | 9.4 | <.001 | |
| .757 | 73.3 | 78.1 | 48.9 | 91.1 | 3.3 | 2.9 | <.001 | |
| Passive abduction | ||||||||
| .867 | 93.3 | 80.0 | 57.1 | 97.7 | 4.7 | 11.9 | <.001 | |
| .686 | 46.7 | 90.5 | 58.3 | 85.6 | 4.9 | 1.7 | .002 | |
| Passive external rotation | ||||||||
| .833 | 93.3 | 73.3 | 50.0 | 97.5 | 3.5 | 10.9 | <.001 | |
| .881 | 93.3 | 82.9 | 60.9 | 97.8 | 5.5 | 12.4 | <.001 | |
| .790 | 66.7 | 91.4 | 69.0 | 90.6 | 7.8 | 2.7 | <.001 | |
| Anterior deltoid < gravity | .810 | 93.3 | 68.6 | 45.9 | 97.3 | 3.0 | 10.2 | <.001 |
| Middle deltoid < gravity | .793 | 96.7 | 61.9 | 42.0 | 98.5 | 2.5 | 18.8 | <.001 |
| Posterior deltoid < gravity | .795 | 93.3 | 65.7 | 43.8 | 97.2 | 2.7 | 9.8 | <.001 |
⁎Cutoff is highest ROC value. |
Table 4. Diagnostic Properties of Predictive Models of Clinical Tests for Early Identification of Patients Who Complained of Hemiplegic Shoulder Pain at Rest (n=30)
| Predictive Models | ROC | Sensitivity | Specificity | PPV | NPV | LR+ | LR− |
|---|---|---|---|---|---|---|---|
| Model A (ROC >0.8) | .999 | 96.7 | 99.0 | 96.7 | 99.0 | 96.7 | 30.0 |
| Neer (+ve), HBN maneuver ≥5, HBB maneuver ≥5, passive abduction >5° difference, passive external rotation >10° difference, anterior deltoid < gravity | |||||||
| Model B (ROC >.85) | .994 | 96.7 | 99.0 | 96.7 | 99.0 | 96.7 | 30.0 |
| Neer (+ve), HBN maneuver ≥5, passive abduction >5° difference, passive external rotation >10° difference | |||||||
| Model C (ROC >.88) | .994 | 96.7 | 99.0 | 96.7 | 99.0 | 96.7 | 30.0 |
| Neer (+ve), HBN maneuver ≥5, passive external rotation >10° diff | |||||||
| Model D (2 clinical tests, 3 versions) | |||||||
| (I): Neer (+ve) and HBN maneuver ≥5 | .991 | 96.7 | 99.0 | 96.7 | 99.0 | 96.7 | 30.0 |
| (II) : Neer (+ve) and passive external rotation >10° difference | .963 | 82.4 | 98.0 | 93.3 | 94.3 | 41.2 | 5.6 |
| (III): HBN maneuver >4 and passive external rotation >10° difference | .992 | 96.7 | 99.0 | 96.7 | 99.0 | 96.7 | 30.0 |
Table 5. Diagnostic Probabilities of Predictive Model C That Can Be Used to Identify Patients With Complaints of Hemiplegic Shoulder Pain at Rest (n=30)
| Neer Test | HBN Maneuver | Passive External Rotation Difference (deg) | Probability (%) |
|---|---|---|---|
| Negative | ≤4 | ≤10 | 0.0 |
| Negative | ≤4 | >10 | 0.0 |
| Negative | ≥5 | ≤10 | 0.0 |
| Negative | ≥5 | >10 | 0.0 |
| Positive | ≤4 | ≤10 | 1.7 |
| Positive | ≤4 | >10 | 11.0 |
| Positive | ≥5 | ≤10 | 84.0 |
| Positive | ≥5 | >10 | 98.0 |
Discussion
The current study found that the proposed predictive model consisting of 3 simple bedside clinical tests allowed clinicians a 98% probability of provisional early diagnosis of hemiplegic shoulder pain after stroke. The clinical tests were positive Neer test, moderate or greater shoulder pain during performance of the HBN maneuver, and a difference of greater than 10° of passive external rotation at the shoulder joint. Highly sensitive tests tend to have low specificity values, whereas highly specific ones have low sensitivity and thus to increase the accuracy of a diagnosis, 2 or more complementary clinical tests are usually performed.38, 39, 41 The combined accuracy of 3 clinical tests in model C had a PPV and sensitivity of 96.7% and a similar likelihood ratio, sensitivity, and specificity values as model A that consisted of 6 clinical tests (see table 4). Moreover, the high standard error (SE) for Neer test (SE=4303.89), and concurrent low error for HBN score of 5 or greater (SE=1.473) and passive external rotation difference of more than 10° (SE=2.022) suggested significant interactions occurred between clinical tests in model C.
Our results confirmed reports of an association between shoulder pain at rest after stroke and decreased shoulder external rotation in the affected shoulder.4, 13, 18, 20, 24, 43, 44, 45 Limitation of shoulder external rotation on the paretic upper limb also correlated with the time of onset of stroke43 (r=−.538, P<.01). The current finding indicated that as early as a week after stroke, 93.3% of patients with hemiplegic shoulder pain at rest had a difference of more than 10° in range of shoulder external rotation between limbs. Although obligatory external rotation is necessary for pain-free gliding of the supraspinatus tendon during arm elevation, 17% of patients who did not complain of hemiplegic shoulder pain also had limitation in shoulder external rotation on their paretic limb (see table 2). Patients with shoulder instability also reported signs of shoulder impingement during arm elevation.46 More investigation is required to evaluate the dynamics that occur at the glenohumeral joint of patients with hemiparetic upper limbs when they perform elevation tasks. Another study from our laboratory is currently studying the shoulder muscle activation patterns among patients with anterior shoulder instability and those with hemiparetic shoulder dysfunction to better understand the neuromotor control strategies that patients adopt during pain-free performance of overhead reaching tasks.
A number of researchers have questioned the accuracy of reporting pain associated with this poorly understood phenomenon of hemiplegic shoulder pain.25, 28, 47 Price et al28 expressed that stroke subtypes influenced the reporting of pain intensity at the shoulder. However, Bohannon and Andrews25 felt that the method of assessing shoulder pain was the most important factor. Constant and Murley34 assessed shoulder pain intensity among orthopedic patients during the performance of functional tasks. In the current study, shoulder pain was also assessed during performance of functional tasks including HBB and HBN maneuvers, and the cutoff intensity level of reporting of shoulder pain was moderate (NRS score ≥5), which was consistent with findings of another study involving 54 patients.24 They too reported that approximately 20% of stroke patients experienced shoulder pain at intensities equal or greater than 5. Currently, there is no reliable criterion standard to accurately evaluate signs of acute shoulder pain.39 The present study found that complaints of moderate pain at rest and 3 positive clinical tests can act as a pseudo-valid standard to identify those who are at risk of hemiplegic shoulder pain. Moreover, the physical therapist’s interrater reliability measurements of shoulder external rotation in the present study (see table 1) were similar to scores reported by Braus et al.22 Our ICC values were also better than .19 and .73 scored by rheumatologists and physical therapists, respectively, when they measured shoulder external rotation during abduction with goniometry40 (see table 1). An ICC value of .89 is deemed to be acceptable for clinical practice.41
Chronic conditions such as complex regional pain syndrome have identified predictive symptoms and their critical levels, and these findings led to better understanding and management of this chronic condition.48 To our knowledge, this study is the first to establish that a combination of 3 simple clinical tests can accurately predict the early onset of shoulder pain after stroke. The results enrich our understanding of the possible pathophysiology associated with this poorly understood yet preventable medical condition. We plan to further evaluate the 3 musculoskeletal tests identified against examination under anesthesia and magnetic resonance imaging of the shoulder, which are deemed to be the criterion standards to evaluate shoulder dysfunction.
Study Limitations
This study quantified pain intensity at the hemiplegic shoulder using an NRS, which is easy to administer and score.30 We adopted this approach because there is no criterion standard to predict the onset of hemiplegic shoulder pain. To minimize false-positive reporting of shoulder pain, the current study raised the cutoff intensity threshold to an NRS score of 5 or more, consistent with practices of others.24 Furthermore, the cuff tightness test verified the ability of patients to discriminate the intensity of pain in the upper limbs. The current study could have used another pain intensity measuring tool to confirm reliability of the NRS, but this would have prolonged the assessment procedure and probably caused frustrated patients to respond inaccurately. We acknowledge that it would be ideal to perform costly investigations such as radiography, magnetic resonance imaging, or ultrasound as criterion standards to evaluate all 135 patients participating in the current study. With the results of the current study, we can now incorporate these investigative procedures for a smaller population of acute stroke patients to evaluate the concurrent validity of the current battery of 3 clinical tests to predict the early onset of hemiplegic shoulder pain. Another possible limitation of the current study was the inclusion of patients who suffer infarctions at various sites of the brain. Although our exclusion criterion eliminated patients with thalamic infarctions and central shoulder pain syndrome, neural reorganization after stroke may have stimulated the thalamus to induce shoulder pain. The unaffected ipsilateral shoulder may also have impaired ranges of shoulder motion and muscle strengths that could provide inaccurate comparisons.49, 50, 51 Finally, there were only 30 patients in the experimental group who met the criteria of moderate hemiplegic shoulder pain. The small number of patients in the experimental group suggests that the current predictive model requires further investigation for universal acceptance. Thus, we are embarking on recruiting more patients to supplement the current study’s data pool.
Conclusions
The study provides 3 simple clinical tests to predict those who are likely to complain of hemiplegic shoulder pain early after stroke. Early diagnosis of this pathology will encourage early intervention and presumably an improved outcome for the patients.
Supplier
Acknowledgments
We thank the physicians and therapists from Tan Tock Seng Hospital, Changi General Hospital, and National University Hospital for their active support during the course of this study.
References
- Medical complication after stroke: a multicenter study. Stroke. 2000;31:1223–1229
- . Medical complications experienced by a cohort of stroke survivors during inpatient, tertiary-level stroke rehabilitation. Arch Phys Med Rehabil. 2004;85:466–469
- . Shoulder pain in people with a stroke: a population-based study. Clin Rehabil. 2003;17:304–311
- . Post stroke shoulder pain: a prospective study of the association and risk factors in 152 patients from a consecutive cohort of 205 patients presenting with stroke. Eur J Pain. 2002;5:467–474
- . Stroke rehabilitation (2. Co-morbidities and complications). Arch Phys Med Rehabil. 1999;80(5 Suppl 1):S8–S16
- . Post stroke shoulder pain: more common than previously realized. Eur J Pain. 2000;4:313–315
- . Recovery of proximal and distal arm weakness in the ipsilateral upper limb after stroke. NeuroRehabilitation. 2002;17:153–159
- . Shoulder pain in acutely admitted hemiplegics. Clin Rehabil. 1994;8:334–340
- . Painful shoulder in hemiplegia. Arch Phys Med Rehabil. 1986;6:22–36
- . Hemiplegic shoulder pain (HSP): natural history and investigation of associated features. Disabil Rehabil. 1996;18:497–501
- . Upper-limb function and recovery in the acute phase of poststroke. J Rehabil Res Dev. 2005;42:65–78
- . The effect of shoulder pain on outcome of acute hemiplegia. Clin Rehabil. 1995;9:21–27
- . Arthrographic and clinical findings in patients with hemiplegic shoulder pain. Arch Phys Med Rehabil. 2003;84:1786–1791
- . Shoulder complex position and glenohumeral subluxation in hemiplegia. Arch Phys Med Rehabil. 1996;76:857–864
- Painful shoulder in the hemiplegic and unilateral neglect. Arch Phys Med Rehabil. 1990;71:673–676
- . Glenohumeral joint subluxation and reflex sympathetic dystrophy in hemiplegic patients. Arch Phys Med Rehabil. 2000;82:944–946
- . Shoulder pain after stroke. Int J Rehabil Res. 1995;18:273–276
- . Evaluation and treatment of shoulder subluxation in hemiplegia. Am J Phys Med Rehabil. 1998;77:421–426
- . Shoulder pain in hemiplegia: statistical relationship with five variables. Arch Phys Med Rehabil. 1986;67:514–516
- . Shoulder pain and subluxation after stroke: correlation or coincidence?. Am J Occup Ther. 1996;50:194–201
- . Little evidence of synovitis in hemiplegic shoulder pain. [abstract] Arch Phys Med Rehabil. 2003;84(9):A39
- . The shoulder-hand syndrome after stroke: a prospective clinical trial. Ann Neuro. 1994;36:728–733
- . Immunolocation of cytokines and their receptors in adhesive capsulitis of the shoulder. J Orthop Res. 1997;15:427–436
- . The long-term outcome of arm function after stroke: results of a follow-up study. Disabil Rehabil. 1999;21:357–364
- . Shoulder subluxation and pain in stroke patients. Am J Occup Ther. 1990;44:507–509
- . The shoulder in hemiplegia. In: Donatelli R editors. Physical therapy in the shoulder. 3rd ed.. New York: Churchill Livingstone; 1997;p. 205–227
- . The painful shoulder: Part 1 (Clinical evaluation). Am Fam Physician. 2000;61:3078–3088
- . Can stroke patients use visual analogue scales?. Stroke. 1999;30:1357–1361
- . Prevalence of shoulder pain in the community: the influence of case definition. Ann Rheum Dis. 1997;56:308–312
- . Assessing global pain severity by self-report in clinical and health services research. Spine. 2000;25:3140–3151
- . Assessment of strength deficits in eight paretic upper extremity muscle groups of stroke patients with hemiplegia. Phys Ther. 1987;67:522–525
- . Reliability of measurement of muscle tone and muscle power in stroke patients. Age Ageing. 2000;29:223–228
- . A review of the properties and limitations of the Ashworth and modified Ashworth Scales as measures of spasticity. Clin Rehabil. 1999;13:373–383
- . A clinical method of functional assessment of the shoulder. Clin Orthop Relat Res. 1987;160–164Jan(214)
- . An assessment of the interexaminer reliability of tests for shoulder instability. J Shoulder Elbow Surg. 2004;13:18–23
- . Clinical examination of the unstable shoulder. Sports Med. 2002;32:447–457
- . The diagnostic value of arthroscopy in glenohumeral instability. J Bone Joint Surg Br. 1990;72:698–700
- . Diagnostic values of clinical diagnostic tests in subacromial impingement syndrome. Ann Rheum Dis. 2000;59:44–47
- . In: Evidence based management of acute musculoskeletal pain. Brisbane: Australian Acad Pr; 2003;p. 119–146
- How reliable do rheumatologists measure shoulder movement?. Ann Rheum Dis. 2002;61:612–616
- . What do we know about the reliability and validity of physical examination tests used to examine the upper extremity?. J Hand Surg [Am]. 1999;24:185–193
- . Stroke in Singapore—an overview. Singapore Med J. 1998;39:564–565
- . Decrease shoulder range of motion on paretic side after stroke. Phys Ther. 1989;69:768–772
- Rajaratnam BS, Luah CY, Saw LA. EMG study of the motor recruitment pattern in hemiparetic shoulder during active shoulder during active shoulder abduction. In: Proceedings of the 13th International Congress of the World Confederation of Physical Therapists; 1999 May 23-28; Yokohama (Japan).
- Rajaratnam BS. Motor recruitment pattern in the hemiplegic shoulder. In: Proceeding of the 3rd National Congress of the Singapore Physiotherapy Association; 1999 May 18; Singapore.
- The anterior tilt of the acromion: radiographic evaluation and correlation with shoulder disease. Eur J Radiol. 1998;8:1639–1646
- . Hemiplegic shoulder pain: defining the problem and its management. Disabil Rehabil. 2001;23:698–705
- . Predictive values of symptoms level measurements for complex regional pain syndrome type 1. Eur J Pain. 2005;9:49–56
- . Kinematic alterations in the ipsilateral shoulder of patients with hemiplegia due to stroke. Am J Phys Med Rehabil. 2005;84:97–105
- . Time and magnitude of torque generation is impaired in both arms following stroke. Muscle Nerve. 2003;28:46–53
- . Abnormal joint torque patterns in the paretic upper limb of subjects with hemiparesis. Muscle Nerve. 2001;24:273–283
- a Version 13.0; SPSS Inc, 233 S Wacker Dr, 11th Fl, Chicago, IL 60606.
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(07)00327-9
doi:10.1016/j.apmr.2007.05.001
© 2007 American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation. Published by Elsevier Inc. All rights reserved.
Volume 88, Issue 8 , Pages 1016-1021, August 2007
