Hemiplegic Shoulder Pain: Associated Factors and Rehabilitation Outcomes of Hemiplegic Patients With and Without Shoulder Pain Ozgur Zeliha Karaahmet, MD,1 Emel Eksioglu, MD,1 Eda Gurcay, MD,1 Pınar Bora Karsli, MD,1 Ugur Tamkan, Psy,1 Ajda Bal, MD,1 and Aytul Cakcı, MD1 1
Department of Physical Medicine & Rehabilitation, Dıskapı Yıldırım Beyazıt Education and Research Hospital, Ankara, Turkey
Objectives: To analyze the incidence of and the factors associated with shoulder pain in people with hemiplegia and to understand the effect of rehabilitation programs on the parameters of motor function and activity limitations in patients with and without hemiplegic shoulder pain. Methods: Patients in the initial 6-month period after stroke who were hospitalized in the physical medicine and rehabilitation clinic were included in the study. Patients were considered early rehabilitation entrants if they were admitted in the first 0 to 30 days after a stroke and late rehabilitation entrants if they were admitted 30 to 120 days after a stroke. Demographic and clinical features, complications, and medical histories of the patients were recorded. Upper extremity Fugl-Meyer Motor Assessment (FMA), Frenchay Arm Test (FAT), and Functional Independence Measure (FIM) were applied to the patients on admission, at discharge, and after 1 month of follow-up. Results: Twenty-one (38%) patients did not have shoulder pain, and 34 (62%) patients had decreased shoulder pain. Immobilization, duration of disease, and late rehabilitation were shown to be effective treatments for shoulder pain. The major risk factors were disease duration and poor initial motor function. In both groups, the FMA, FAT, and FIM scores showed significant changes. This improvement did not differ between the 2 groups. Conclusion: Duration of disease and low motor functional capacities have the most important impact on shoulder pain. In patients with and without shoulder pain, a systematic rehabilitation program is beneficial with respect to motor function and daily living activities. Key words: hemiplegic shoulder pain, stroke rehabilitation
H
emiplegic shoulder pain (HSP) in patients with stroke is a common and disabling complication, interfering with both function and quality of life. The history and examination of these patients suggest that the cause of the pain is multifactorial and includes features of both neurological and musculoskeletal pathology.1 Subsequently, HSP may develop in approximately 16% to 72% of patients. In patients with involuntary movement in the affected extremities, this proportion may increase up to 80%.2 The underlying causes and sources of HSP have been the subject of debate and research for years. Kalichman and Ratmansky3 conducted a literature review to better understand the underlying mechanism of HSP and the factors contributing to its development. HSP Corresponding author: Ozgur Zeliha Karaahmet, MD, Department of Physical Medicine & Rehabilitation, Dıs¸kapı Yıldırım Beyazıt Education and Research Hospital, 06080 Altındag- Ankara, Turkey; phone: +90-505-815-1585; fax: +90-312-318-6690; e-mail: [email protected]
was categorized on the basis of 3 underlying aspects: impaired motor control, soft tissue lesions, and altered peripheral and central nervous system activity. Kalichman and Ratmansky3 concluded that these factors may occur separately, coexist simultaneously, or evolve during the rehabilitation period with each triggering development of another. In addition, many other previous studies examined risk factors of HSP, such as shoulder spasticity, shoulder subluxation, and rotator cuff lesions.4-6 Because the etiology of HSP still remains unknown, this study was designed to elicit all possible causes and risk factors in detail. The aims of this study were to investigate the incidence of and the factors associated with shoulder pain in patients with hemiplegia and to examine the effects Top Stroke Rehabil 2014;21(3):237–245 © 2014 Thomas Land Publishers, Inc. www.strokejournal.com doi: 10.1310/tsr2103-237
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of rehabilitation on motor function and activity limitations in patients with and without HSP. Methods A total of 63 patients with stroke attending the physical medicine and rehabilitation clinic were enrolled in this study. Study participation was totally voluntary, and patients were informed about the nature of the study. Oral approvals were obtained from each participant before the study began. All procedures were in accordance with the Declaration of Helsinki. The study was approved by the local institutional ethical committee. Patients with stroke who were hospitalized in the rehabilitation clinic no later than 120 days after stroke with hemorrhagic or thromboembolic cerebrovascular disease and with Brunnstrom stage 1-4 initially were included in the study. Unconscious patients and patients with recurrent stroke or bilateral hemiplegia were excluded from the study. Patients who were admitted to the hospital within 0 to 30 and 30 to 120 days from the date of stroke were considered as early and late rehabilitation entrants, respectively. Age, gender, handedness, hemiplegic side, disease duration, and cause of stroke were recorded. Additionally, patients were evaluated for the presence of impingement, soft tissue injury, rotator cuff tears, shoulder-hand syndrome, brachial plexus and peripheral nerve injuries, neglect, aphasia, spasticity, subluxation, and depression. HSP was determined when a patient reported pain in the shoulder region of the hemiplegic side in the resting state or during passive range-ofmotion (ROM) exercise.6 Pain value was noted as present or absent. Impingement syndrome, soft tissue injury, and rotator cuff tears were diagnosed by clinical evaluation and ultrasonographic findings. Brachial plexus and peripheral nerve injuries were evaluated by electrophysiological studies. A diagnosis of shoulder-hand syndrome was primarily based on the clinical entity and International Association of Science Parks criteria.7 The presence of hemineglect was determined by using the Star Cancellation Test.8 The Star Cancellation Test is a screening tool that was developed to detect the presence of unilateral spatial neglect in the near extrapersonal space in
patients with stroke. It involves patients searching for stars and marking them with a pen on a sheet of paper. Patients with right-hemisphere neglect often start on the right side of the page and omit stars on the left of the page, whereas control subjects who read from left to right usually start on the left. The Star Cancellation Test is the single most sensitive bedside test for hemineglect. Aphasia was evaluated according to the Frenchay Aphasia Screening Test. The Frenchay Aphasia Screening Test is a reliable test that can be used by nonspecialists to discriminate between aphasia and normal language. It takes approximately 3 to 10 minutes to administer and covers auditory comprehension, reading comprehension (receptive domains), and expressive language and writing (expressive domains). Scores on the Frenchay Aphasia Screening Test range from 0 to 30; higher scores indicate better language skills.9 The Modified Ashworth Scale (MAS) was used to measure spasticity.10 The MAS is a measure of spasticity that ranges from 0 to 4, with 0 indicating normal muscle tone and 4 suggesting rigidity of effector parts in flexion or extension of elbow flexors and in external rotation of the subscapularis muscle. Patients who scored >1 on the scale were considered to have spasticity. Patients were evaluated during early and late rehabilitation and underwent shoulder examinations and spasticity measurements at 3 intervals: on admission, at discharge, and 1 month after discharge (at follow-up). All outcome measurements were made by the same physician. Subjects who had HSP during the rehabilitation period were separated from the rest of the patients, and factors associated with the pain were investigated. Analyses of shoulder subluxation were carried out during the physical examination through the measurement of the subacromial space in finger’s breadth. Subluxation was graded as “existent” when at least half a finger could be placed between the acromion and the humerus.11 The motor functionality of the upper extremity was analyzed by using the Fugl-Meyer Motor Assessment (FMA) 12 and Frenchay Arm Test (FAT).13 Functional status was assessed by the Functional Independence Measure (FIM).14 The FMA is used in clinical trials and rehabilitation settings that treat people after stroke
Hemiplegic Shoulder Pain
and is one of the most widely used quantitative measures of motor impairment. Each item on the FMA is rated on a 3-point ordinal scale (0 = cannot perform, 1 = performs partially, 2 = performs fully), and items measure motor performance, sensory function, balance, joint range of motion, and joint pain. The upper extremity motor function portion of the FMA is used in this study (maximum score is 66).12 The FAT is a simple measurement of arm function and is suitable for use with patients recovering from stroke. It takes less than 3 minutes to complete and consists of 5 tasks. The patient receives a score of 1 for each task completed successfully. The patient sits at a table with hands in his or her lap and begins each task from this position.13 The FIM scale assesses physical and cognitive disability. This scale focuses on the burden of care. Items are scored on the level of assistance required for an individual to perform activities of daily living. The scale includes 18 items. Each item is scored from 1 to 7 based on level of independence: 1 represents total dependence and 7 indicates complete independence. Possible scores range from 18 to 126.14 In addition, the Beck Depression Inventory (BDI), a self-report inventory, was used to examine the emotional stability of patients. The BDI is one of the most widely used instruments for measuring the severity of depression. It consists of 21 items. Each item is a list of 4 statements arranged in increasing severity about a particular symptom of depression. The BDI grades depression as minimal (0-13), mild (14-19), moderate (20-28), and severe (29-36).15,16 For the rehabilitation program, all patients were invited to the clinic 5 days a week for 1 month. Both conventional and neurophysiological treatment methods (Brunnstrom, Bobath techniques) were used. Initially, education was provided to the patients’ relatives or caregivers for the protection and positioning of the hemiplegic shoulder. ROM exercises were started in the early period and performed within the limits of painless motion without exceeding the level of the head. Waist belt, shoulder strap, and banding were used for patients with flaccid shoulder. Analgesics were administered (subacromial or intraarticular
239
injection), and physical therapy was provided for patients with shoulder pain. Statistical analyses were performed using the commercial IBM SPSS for Windows version 11.5 (IBM Corp., Armonk, NY). Yates’ chi-square and Fisher exact tests were used to assess the qualitative differences within groups. Alternatively, numeric variables were detected using Student t test and the Mann-Whitney U test. Descriptive statistics were presented as median with interquartile range in the FMA, FAT, and FIM. The Friedman test was used to determine whether there was a statistically significant change within groups in FMA, FAT, and FIM. A P value < .025 was considered indicative of statistical significance. The particular follow-up periods associated with the significance detected by the Friedman test were determined using the Bonferroni-corrected Wilcoxon test. For this analysis, a P value .05). The effects of complications on patients with HSP are shown in Table 2. Premorbid shoulder pain, previous trauma, and sedentary lifestyle were not associated with the development of HSP (P > .05). Evaluation of the effect of the timing of rehabilitation on HSP revealed that a late start to rehabilitation significantly increased the risk Table 1. Upper extremity complications on admission and discharge from the hospital Complications
Admission, n (%)
Discharge, n (%)
Subluxation Atrophy Shoulder-hand syndrome Brachial plexus lesion Fracture Spasticity Impingement Adhesive capsulitis
5 (9.1) 4 (7.3) 1 (1.8) 1 (1.8) 1 (1. 8) 5 (9.1) 5 (9.1) 4 (7.3)
9 (16.4) 4 (7.3) 1 (1.8) 1 (1.8) 1 (1.8) 19 (34.5) 19 (34.5) 13 (34.5)
Table 2. Effects of complications on patients with HSP HSP
Neglect Aphasia Depression Spasticity Sensory disturbance Subluxation
+ – + – + – + – + – + –
+ (%)
– (%)
P value
9 (90) 25 (55.6) 7 (55.6) 27 (61.4) 13 (65) 21 (60) 15 (78.9) 19 (52.8) 4 (40) 30 (66.7) 7 (77.8) 27 (58.7)
1 (10) 20 (44.4) 4 (36.4) 17 (38.6) 7 (35) 14 (40) 4 (21.1) 17 (47.2) 6 (60) 15 (33.3) 2 (22.2) 19 (41.3)
.07 1 .77 .82 .15 .45
Note: HSP = hemiplegic shoulder pain.
of HSP development [χ2(1, N = 55) = 5,723; P = .017; P < .05]. Disease duration and magnitude of HSP were positively correlated (U = 208.50; P = .002; P .05). In patients without HSP, a statistically significant change was observed over time in terms of FMA total scores. FMA scores were significantly higher at discharge and follow-up than at admission (both Ps = .003). Moreover, FMA scores were significantly higher at follow-up than at discharge (P
Department of Physical Medicine & Rehabilitation, Dıskapı Yıldırım Beyazıt Education and Research Hospital, Ankara, Turkey
Objectives: To analyze the incidence of and the factors associated with shoulder pain in people with hemiplegia and to understand the effect of rehabilitation programs on the parameters of motor function and activity limitations in patients with and without hemiplegic shoulder pain. Methods: Patients in the initial 6-month period after stroke who were hospitalized in the physical medicine and rehabilitation clinic were included in the study. Patients were considered early rehabilitation entrants if they were admitted in the first 0 to 30 days after a stroke and late rehabilitation entrants if they were admitted 30 to 120 days after a stroke. Demographic and clinical features, complications, and medical histories of the patients were recorded. Upper extremity Fugl-Meyer Motor Assessment (FMA), Frenchay Arm Test (FAT), and Functional Independence Measure (FIM) were applied to the patients on admission, at discharge, and after 1 month of follow-up. Results: Twenty-one (38%) patients did not have shoulder pain, and 34 (62%) patients had decreased shoulder pain. Immobilization, duration of disease, and late rehabilitation were shown to be effective treatments for shoulder pain. The major risk factors were disease duration and poor initial motor function. In both groups, the FMA, FAT, and FIM scores showed significant changes. This improvement did not differ between the 2 groups. Conclusion: Duration of disease and low motor functional capacities have the most important impact on shoulder pain. In patients with and without shoulder pain, a systematic rehabilitation program is beneficial with respect to motor function and daily living activities. Key words: hemiplegic shoulder pain, stroke rehabilitation
H
emiplegic shoulder pain (HSP) in patients with stroke is a common and disabling complication, interfering with both function and quality of life. The history and examination of these patients suggest that the cause of the pain is multifactorial and includes features of both neurological and musculoskeletal pathology.1 Subsequently, HSP may develop in approximately 16% to 72% of patients. In patients with involuntary movement in the affected extremities, this proportion may increase up to 80%.2 The underlying causes and sources of HSP have been the subject of debate and research for years. Kalichman and Ratmansky3 conducted a literature review to better understand the underlying mechanism of HSP and the factors contributing to its development. HSP Corresponding author: Ozgur Zeliha Karaahmet, MD, Department of Physical Medicine & Rehabilitation, Dıs¸kapı Yıldırım Beyazıt Education and Research Hospital, 06080 Altındag- Ankara, Turkey; phone: +90-505-815-1585; fax: +90-312-318-6690; e-mail: [email protected]
was categorized on the basis of 3 underlying aspects: impaired motor control, soft tissue lesions, and altered peripheral and central nervous system activity. Kalichman and Ratmansky3 concluded that these factors may occur separately, coexist simultaneously, or evolve during the rehabilitation period with each triggering development of another. In addition, many other previous studies examined risk factors of HSP, such as shoulder spasticity, shoulder subluxation, and rotator cuff lesions.4-6 Because the etiology of HSP still remains unknown, this study was designed to elicit all possible causes and risk factors in detail. The aims of this study were to investigate the incidence of and the factors associated with shoulder pain in patients with hemiplegia and to examine the effects Top Stroke Rehabil 2014;21(3):237–245 © 2014 Thomas Land Publishers, Inc. www.strokejournal.com doi: 10.1310/tsr2103-237
237
238
TOPICS IN STROKE REHABILITATION/MAY-JUNE 2014
of rehabilitation on motor function and activity limitations in patients with and without HSP. Methods A total of 63 patients with stroke attending the physical medicine and rehabilitation clinic were enrolled in this study. Study participation was totally voluntary, and patients were informed about the nature of the study. Oral approvals were obtained from each participant before the study began. All procedures were in accordance with the Declaration of Helsinki. The study was approved by the local institutional ethical committee. Patients with stroke who were hospitalized in the rehabilitation clinic no later than 120 days after stroke with hemorrhagic or thromboembolic cerebrovascular disease and with Brunnstrom stage 1-4 initially were included in the study. Unconscious patients and patients with recurrent stroke or bilateral hemiplegia were excluded from the study. Patients who were admitted to the hospital within 0 to 30 and 30 to 120 days from the date of stroke were considered as early and late rehabilitation entrants, respectively. Age, gender, handedness, hemiplegic side, disease duration, and cause of stroke were recorded. Additionally, patients were evaluated for the presence of impingement, soft tissue injury, rotator cuff tears, shoulder-hand syndrome, brachial plexus and peripheral nerve injuries, neglect, aphasia, spasticity, subluxation, and depression. HSP was determined when a patient reported pain in the shoulder region of the hemiplegic side in the resting state or during passive range-ofmotion (ROM) exercise.6 Pain value was noted as present or absent. Impingement syndrome, soft tissue injury, and rotator cuff tears were diagnosed by clinical evaluation and ultrasonographic findings. Brachial plexus and peripheral nerve injuries were evaluated by electrophysiological studies. A diagnosis of shoulder-hand syndrome was primarily based on the clinical entity and International Association of Science Parks criteria.7 The presence of hemineglect was determined by using the Star Cancellation Test.8 The Star Cancellation Test is a screening tool that was developed to detect the presence of unilateral spatial neglect in the near extrapersonal space in
patients with stroke. It involves patients searching for stars and marking them with a pen on a sheet of paper. Patients with right-hemisphere neglect often start on the right side of the page and omit stars on the left of the page, whereas control subjects who read from left to right usually start on the left. The Star Cancellation Test is the single most sensitive bedside test for hemineglect. Aphasia was evaluated according to the Frenchay Aphasia Screening Test. The Frenchay Aphasia Screening Test is a reliable test that can be used by nonspecialists to discriminate between aphasia and normal language. It takes approximately 3 to 10 minutes to administer and covers auditory comprehension, reading comprehension (receptive domains), and expressive language and writing (expressive domains). Scores on the Frenchay Aphasia Screening Test range from 0 to 30; higher scores indicate better language skills.9 The Modified Ashworth Scale (MAS) was used to measure spasticity.10 The MAS is a measure of spasticity that ranges from 0 to 4, with 0 indicating normal muscle tone and 4 suggesting rigidity of effector parts in flexion or extension of elbow flexors and in external rotation of the subscapularis muscle. Patients who scored >1 on the scale were considered to have spasticity. Patients were evaluated during early and late rehabilitation and underwent shoulder examinations and spasticity measurements at 3 intervals: on admission, at discharge, and 1 month after discharge (at follow-up). All outcome measurements were made by the same physician. Subjects who had HSP during the rehabilitation period were separated from the rest of the patients, and factors associated with the pain were investigated. Analyses of shoulder subluxation were carried out during the physical examination through the measurement of the subacromial space in finger’s breadth. Subluxation was graded as “existent” when at least half a finger could be placed between the acromion and the humerus.11 The motor functionality of the upper extremity was analyzed by using the Fugl-Meyer Motor Assessment (FMA) 12 and Frenchay Arm Test (FAT).13 Functional status was assessed by the Functional Independence Measure (FIM).14 The FMA is used in clinical trials and rehabilitation settings that treat people after stroke
Hemiplegic Shoulder Pain
and is one of the most widely used quantitative measures of motor impairment. Each item on the FMA is rated on a 3-point ordinal scale (0 = cannot perform, 1 = performs partially, 2 = performs fully), and items measure motor performance, sensory function, balance, joint range of motion, and joint pain. The upper extremity motor function portion of the FMA is used in this study (maximum score is 66).12 The FAT is a simple measurement of arm function and is suitable for use with patients recovering from stroke. It takes less than 3 minutes to complete and consists of 5 tasks. The patient receives a score of 1 for each task completed successfully. The patient sits at a table with hands in his or her lap and begins each task from this position.13 The FIM scale assesses physical and cognitive disability. This scale focuses on the burden of care. Items are scored on the level of assistance required for an individual to perform activities of daily living. The scale includes 18 items. Each item is scored from 1 to 7 based on level of independence: 1 represents total dependence and 7 indicates complete independence. Possible scores range from 18 to 126.14 In addition, the Beck Depression Inventory (BDI), a self-report inventory, was used to examine the emotional stability of patients. The BDI is one of the most widely used instruments for measuring the severity of depression. It consists of 21 items. Each item is a list of 4 statements arranged in increasing severity about a particular symptom of depression. The BDI grades depression as minimal (0-13), mild (14-19), moderate (20-28), and severe (29-36).15,16 For the rehabilitation program, all patients were invited to the clinic 5 days a week for 1 month. Both conventional and neurophysiological treatment methods (Brunnstrom, Bobath techniques) were used. Initially, education was provided to the patients’ relatives or caregivers for the protection and positioning of the hemiplegic shoulder. ROM exercises were started in the early period and performed within the limits of painless motion without exceeding the level of the head. Waist belt, shoulder strap, and banding were used for patients with flaccid shoulder. Analgesics were administered (subacromial or intraarticular
239
injection), and physical therapy was provided for patients with shoulder pain. Statistical analyses were performed using the commercial IBM SPSS for Windows version 11.5 (IBM Corp., Armonk, NY). Yates’ chi-square and Fisher exact tests were used to assess the qualitative differences within groups. Alternatively, numeric variables were detected using Student t test and the Mann-Whitney U test. Descriptive statistics were presented as median with interquartile range in the FMA, FAT, and FIM. The Friedman test was used to determine whether there was a statistically significant change within groups in FMA, FAT, and FIM. A P value < .025 was considered indicative of statistical significance. The particular follow-up periods associated with the significance detected by the Friedman test were determined using the Bonferroni-corrected Wilcoxon test. For this analysis, a P value .05). The effects of complications on patients with HSP are shown in Table 2. Premorbid shoulder pain, previous trauma, and sedentary lifestyle were not associated with the development of HSP (P > .05). Evaluation of the effect of the timing of rehabilitation on HSP revealed that a late start to rehabilitation significantly increased the risk Table 1. Upper extremity complications on admission and discharge from the hospital Complications
Admission, n (%)
Discharge, n (%)
Subluxation Atrophy Shoulder-hand syndrome Brachial plexus lesion Fracture Spasticity Impingement Adhesive capsulitis
5 (9.1) 4 (7.3) 1 (1.8) 1 (1.8) 1 (1. 8) 5 (9.1) 5 (9.1) 4 (7.3)
9 (16.4) 4 (7.3) 1 (1.8) 1 (1.8) 1 (1.8) 19 (34.5) 19 (34.5) 13 (34.5)
Table 2. Effects of complications on patients with HSP HSP
Neglect Aphasia Depression Spasticity Sensory disturbance Subluxation
+ – + – + – + – + – + –
+ (%)
– (%)
P value
9 (90) 25 (55.6) 7 (55.6) 27 (61.4) 13 (65) 21 (60) 15 (78.9) 19 (52.8) 4 (40) 30 (66.7) 7 (77.8) 27 (58.7)
1 (10) 20 (44.4) 4 (36.4) 17 (38.6) 7 (35) 14 (40) 4 (21.1) 17 (47.2) 6 (60) 15 (33.3) 2 (22.2) 19 (41.3)
.07 1 .77 .82 .15 .45
Note: HSP = hemiplegic shoulder pain.
of HSP development [χ2(1, N = 55) = 5,723; P = .017; P < .05]. Disease duration and magnitude of HSP were positively correlated (U = 208.50; P = .002; P .05). In patients without HSP, a statistically significant change was observed over time in terms of FMA total scores. FMA scores were significantly higher at discharge and follow-up than at admission (both Ps = .003). Moreover, FMA scores were significantly higher at follow-up than at discharge (P
