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Stroke. 1995;26:2277-2280

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(Stroke. 1995;26:2277-2280.)
© 1995 American Heart Association, Inc.


Articles

Prediction of Reflex Sympathetic Dystrophy in Hemiplegic Patients by Electromyographic Study

Pao-Tsai Cheng, MD Chang-Zern Hong, MD

From the Department of Physical Medicine and Rehabilitation, Chang Gung Memorial Hospital, Chang Gung College of Medicine and Technology, Taiwan (P.-T.C.), and the Department of Physical Medicine and Rehabilitation, University of California, Irvine (C.-Z.H).

Correspondence to Pao-Tsai Cheng, MD, Department of Physical Medicine and Rehabilitation, Chang Gung Memorial Hospital, 5 Fu-Hsing St, Kuei-Shan Hsiang, Tao-Yuan, Taiwan.


*    Abstract
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Background and Purpose This study was designed to investigate the correlation between reflex sympathetic dystrophy syndrome (RSDS) in hemiplegic patients and spontaneous electromyographic (EMG) activity, as well as to determine the predictive value of spontaneous EMG activity in early diagnosis of RSDS.

Methods An EMG and nerve conduction velocity study of the weak upper limb was conducted on 70 hemiplegic patients at 3 to 4 weeks after cerebrovascular disease (either cerebral hemorrhage or infarction). Clinical assessment for development of the RSDS was done during the following 6 months. The correlation of RSDS development with the presence of spontaneous EMG activity and certain clinical parameters (including sex, age, side affected, cause of stroke, sensory impairment, spasticity, and shoulder subluxation) was analyzed statistically.

Results Of the 46 patients who exhibited spontaneous activity, 30 (65%) developed clinical RSDS in their hemiplegic upper extremity, whereas only 1 (4%) of the other 24 patients with no spontaneous EMG activity developed clinical RSDS within 6 months after the onset of hemiplegia (P<.001). The correlation of RSDS development with the presence of shoulder subluxation and sensory impairment in the hemiplegic side was statistically significant. Neither age, sex, severity of spasticity, nor etiology of stroke had a significant correlation with the development of clinical RSDS.

Conclusions There is significant correlation between the presence of spontaneous EMG activity and the development of clinical RSDS in the hemiplegic upper extremity after stroke. It is concluded that spontaneous EMG activity in the hemiplegic hands of stroke patients might be a good predictor of the future development of clinical RSDS.


Key Words: electromyography • hemiplegia • reflex sympathetic dystrophy


*    Introduction
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Reflex sympathetic dystrophy syndrome (RSDS), or shoulder-hand syndrome, has been considered one of the major causes of chronic severe shoulder pain after stroke.1 2 3 4 5 6 7 RSDS is a clinical entity with numerous synonyms that is characterized by burning pain, hyperesthesia, swelling, and dystrophic changes in the skin and bone of the affected extremity. Rehabilitation in hemiplegic patients is often severely hampered by the development of RSDS, leading to a prolonged and at times permanent disability. Early recognition and treatment of RSDS are important to provide treatment. However, the diagnosis of RSDS may be difficult to confirm by objective measures. The three-phase technetium bone scan is used to confirm the clinical suspicion of RSDS.8 9 10 Tepperman et al8 reported a 25% incidence of RSDS found by bone scan, concluding that it was a safe and relatively noninvasive procedure and was more sensitive than clinical evaluation for early diagnosis of RSDS after stroke. Weiss et al9 also reported that bone scans might be a good predictor of risk of developing clinical RSDS after stroke. In a previous study, Cheng et al11 found a high incidence of spontaneous electromyographic (EMG) activity in poststroke patients with shoulder-hand syndrome. The purpose of this study was to define the correlation between RSDS and spontaneous EMG activity and to determine its predictive value in early diagnosis of RSDS.


*    Subjects and Methods
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Subjects
All hemiplegic patients (secondary to newly developed stroke, confirmed clinically by head CT) who were admitted to the rehabilitation ward of a general hospital within 3 weeks after onset of stroke were initially evaluated for inclusion in this study. A standard medical history was obtained, including details of stroke and history of shoulder problems. Those patients with recurrent stroke or with known diseases that may cause neuropathy, such as diabetes mellitus, chronic alcoholism, or renal failure, were excluded from this study. Patients with premorbid shoulder arthropathy, shoulder trauma, or brachial plexopathy or patients whose aphasia was too severe to permit an adequate evaluation were also excluded. A total of 70 patients (40 men and 30 women; age range, 42 to 80 years; mean age, 62.3 years) consented to be involved in this study. Thirty-three patients had cerebral hemorrhage, and 37 had cerebral infarction.

Electrodiagnostic Procedures
All 70 patients underwent needle EMG examination of the hemiplegic upper extremity and a motor nerve conduction study of bilateral median nerves at 3 to 4 weeks after onset of hemiplegia. Nicolet Viking IIe EMG apparatus was used. The concentric needle was inserted into the muscles of the hemiplegic upper extremity, including the abductor pollicis brevis, abductor digiti minimi, and extensor digitorum communis. The above muscles were selected based on the findings of a previous study.11

Spontaneous activity was quantitatively recorded for each examined muscle with the following grading system: absent, no spontaneous activity; few, spontaneous activity present at one or two sites for longer than 1 second after moving the needle electrode; moderate, present in three or four sites for longer than 1 second; and many, present in more than four sites for longer than 2 seconds or continuously at all sites.12 13

We conducted a median motor nerve conduction study using a standard technique.13 The compound muscle action potential (CMAP) amplitude and distal latency of median nerve in affected side were compared with the unaffected side.

Assessment of RSDS
The clinical diagnosis of RSDS was based on (1) shoulder pain at rest or with mobilization, (2) swelling of wrist and hand, (3) vasomotor change in the hand, and (4) tenderness to palpation of wrist, metacarpopharyngeal, and interpharyngeal joints.

All 70 patients were assigned to one of the following groups according to Tepperman et al8 at the time of EMG study and follow-up: (1) definite RSDS, showing all shoulder and hand criteria; (2) probable RSDS, showing all hand criteria without shoulder involvement; (3) possible RSDS, displaying hand swelling with metacarpopharyngeal and/or wrist tenderness; and (4) non-RSDS. The first three groups were considered "clinical RSDS."

Clinical Assessment at the Time of Follow-up
Physical and neurological examinations were performed at the time of EMG study as well as at a later follow-up at 6 months; motor and sensory function, the presence of spasticity, passive range of motion of the shoulder in all planes, the intensity of pain with shoulder motion or tenderness by palpation, and the presence of hand swelling and shoulder subluxation were recorded. The clinical data and the appearance of spontaneous EMG activity were then correlated with the presence of RSDS.

Data Analysis
Statistically, the data were analyzed for association among variables, with the {chi}2 test and Fisher's exact test used for small sample size. Student's t test was also used for data analysis. A value of P<.05 was considered significant.


*    Results
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Incidence of RSDS
At the time of EMG examination, only 5 of the 70 patients had clinical RSDS. However, at follow-up evaluation 15 patients had clinically definite RSDS, 9 had probable RSDS, and 7 had possible RSDS (31 patients were considered to have clinical RSDS).

Correlation Between RSDS and Clinical Characteristics
The correlation of development of RSDS with clinical characteristics of the 70 hemiplegic patients at follow-up evaluation is shown in Table 1Down. Hemiplegic patients with sensory impairment and/or shoulder subluxation had a higher incidence of RSDS. Patients with left hemiplegia patients had an increased risk of RSDS, although this did not reach statistical significance. Neither age, sex, severity of spasticity, or cause of stroke had any bearing on subsequent RSDS development.


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Table 1. Correlation of Development of RSDS With Other Clinical Variables of Stroke

Correlation Between RSDS and EMG Findings
Table 2Down shows the correlation between the presence of spontaneous EMG activity and the probability of developing RSDS. Thirty of the 31 patients (97%) with clinical RSDS had EMG evidence of fibrillation or positive sharp wave compared with 16 non-RSDS patients (41%). On the other hand, of the 46 patients who displayed few, moderate, or many instances of spontaneous EMG activity in the hemiplegic hand, 30 (65%) later developed clinical RSDS. Only 1 (4%) of the other 24 patients with no spontaneous EMG activity developed clinical RSDS afterward. A significant correlation (P<.001) was found: the larger the amount of spontaneous EMG activity that appeared, the higher the incidence of subsequently developed RSDS.


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Table 2. Correlation of Presence of Spontaneous EMG Activity With Development of Clinical RSDS in 70 Hemiplegic Patients

Correlation Between RSDS and Nerve Conduction Study
The mean CMAP amplitude was lower in the hemiplegic hand compared with the healthy side. The thenar CMAP amplitude difference between the hemiplegic and healthy sides was larger for the patients who subsequently developed clinical RSDS than for those without RSDS, although it did not reach statistical significance (P=.0668). The difference in distal latency was not statistically significant (P>.5).


*    Discussion
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*Discussion
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RSDS is a painful and disabling condition seen in a paralyzed upper extremity after stroke. Chalsen et al3 reported that 61% of hemiplegic patients had RSDS in the hemiplegic upper extremity, whereas Davis and associates1 found that only 12.5% had RSDS in their series. In this study 31 patients (44%) met the criteria of Tepperman et al8 for definite, probable, or possible RSDS at the follow-up evaluation 6 months after onset of stroke.

Although some earlier authors have reported seeing no spontaneous activity on EMG examination of hemiplegic extremities after stroke,14 15 16 most authors have observed spontaneous EMG activity in hemiplegic limbs,11 17 18 19 20 21 especially in the distal muscles of the paralyzed upper extremity.11 17 18 Cheng et al11 found a close correlation between spontaneous EMG activity and poststroke shoulder-hand syndrome, with spontaneous EMG activity primarily in the abductor pollicis brevis, abductor digiti minimi, and extensor digitorum communis. Our study further confirms the correlation between spontaneous EMG activity and the later development of RSDS. Almost all the patients who had no EMG evidence of spontaneous activity did not develop RSDS, and those with more spontaneous EMG activity had a higher incidence of RSDS. This suggests that spontaneous EMG activity might be a good predictor of the risk of developing clinical RSDS after stroke.

The etiology of RSDS is still unknown. Hooshmand22 reported that the origins of sympathetic pain include inactivity, impaired circulation, and damaged peripheral nerve. A paralyzed shoulder may be overstretched during transfer of a patient, particularly when a patient has concomitant loss of central proprioception. Many authors have suspected a possible brachial plexus lesion related to a hemiplegic shoulder. Partial nerve root avulsions are quite frequently accompanied by spontaneous pathological hyperpathic pain and RSDS.23

Chalsen et al3 and Griffen7 reported that patients with decreased sensation and/or shoulder subluxation in the hemiplegic upper extremity had a higher probability of developing RSDS. Our study confirmed this finding. One may speculate that a hemiplegic patient with sensory impairment and/or shoulder subluxation may have higher incidence of brachial plexus injury, which subsequently causes RSDS. In this study the mean CMAP amplitude, which was diminished in the hemiplegic hand, was similar to findings in previous reports.19 20 It was also found that the difference in CMAP amplitude between hemiplegic and healthy sides is higher for the clinical RSDS group than for the non-RSDS group (although the difference is not statistically significant). These findings are in agreement with the studies cited above, although some studies did not support that hypothesis.24

Joynt5 and Weiss et al9 reported that patients with left hemiplegia had a greater tendency to develop RSDS. In this study patients with left hemiplegia did show an increased tendency to develop RSDS compared with patients with right hemiplegia, but the difference was not statistically significant. As for age, sex, spasticity of the hemiplegic limb, or cause of stroke, no clear relation to clinical RSDS development was found.

In conclusion, for those patients who were asymptomatic for RSDS at the time of EMG examination within the first month after stroke, the appearance of diffuse spontaneous EMG activity may be a good predictor of the future development of clinical RSDS. More research in a larger population may be helpful to confirm this hypothesis. Early aggressive measures to prevent and/or diagnose RSDS for these high-risk patients are particularly important.

Received July 10, 1995; revision received September 1, 1995; accepted September 1, 1995.


*    References
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up arrowAbstract
up arrowIntroduction
up arrowSubjects and Methods
up arrowResults
up arrowDiscussion
*References
 
1. Davis SW, Petrillo CR, Eichberg RD, Chu DS. Shoulder-hand syndrome in a hemiplegic population: a 5-year retrospective study. Arch Phys Med Rehabil. 1977;58:353-356. [Medline] [Order article via Infotrieve]

2. Andersen LT. Shoulder pain in hemiplegia. Am J Occup Ther.. 1985;39:11-19. [Medline] [Order article via Infotrieve]

3. Chalsen GG, Fitzpatrick KA, Navia RA, Bean SA, Reding MJ. Prevalence of the shoulder-hand pain syndrome in an in-patient stroke rehabilitation population: a quantitative cross-sectional study. J Neurol Rehab. 1987;1:137-141.

4. Van Ouwenaller C, Laplace PM, Chantraine A. Painful shoulder in hemiplegia. Arch Phys Med Rehabil. 1986;67:23-26. [Medline] [Order article via Infotrieve]

5. Joynt RL. The source of shoulder pain in hemiplegia. Arch Phys Med Rehabil. 1992;73:409-413. [Medline] [Order article via Infotrieve]

6. Escobar P. Reflex sympathetic dystrophy. Orthop Rev. 1986;15:646-651. [Medline] [Order article via Infotrieve]

7. Griffin JW. Hemiplegic shoulder pain. Phys Ther.. 1986;66:1884-1893.

8. Tepperman PS, Greyson ND, Hilbert L, Jimenez J, Williams JI. Reflex sympathetic dystrophy in hemiplegia. Arch Phys Med Rehabil. 1984;65:442-447. [Medline] [Order article via Infotrieve]

9. Weiss L, Alfano A, Bardfeld P, Weiss J, Friedmann LW. Prognostic value of triple phase bone scanning for reflex sympathetic dystrophy in hemiplegia. Arch Phys Med Rehabil. 1993;74:716-719. [Medline] [Order article via Infotrieve]

10. Davidoff G, Werner R, Cremer S, Jackson MD, Ventocilla C, Wolf L. Predictive value of the three-phase technetium bone scan in diagnosis of reflex sympathetic dystrophy syndrome. Arch Phys Med Rehabil. 1989;70:135-137. [Medline] [Order article via Infotrieve]

11. Cheng PT, Lee CE, Liaw MY, Wong MK. Electrophysiological study of shoulder pain in stroke patients. J Rehabil Med Assoc. 1994;22:67-74.

12. Johnson EW, Denny ST, Kelley JP. Sequence of electromyographic abnormalities in stroke syndrome. Arch Phys Med Rehabil. 1975;56:468-473. [Medline] [Order article via Infotrieve]

13. Kimura J. Electrodiagnosis in Diseases of Nerve and Muscle: Principles and Practice. Philadelphia, Pa: FA Davis Co; 1989:249-274.

14. Alpert S, Idarroga S, Orbegozo J, Rosenthal A. Absence of electromyographic evidence of lower motor neuron involvement in hemiplegic patients. Arch Phys Med Rehabil. 1971;52:179-181. [Medline] [Order article via Infotrieve]

15. Alpert S, Jarrett S, Lerner I, Rosenthal A. Electromyographic findings in early hemiplegia. Arch Phys Med Rehabil. 1973;54:464-465. [Medline] [Order article via Infotrieve]

16. Rizk TE, Christopher RP, Pianls RS, Salazar JE, Higgins C. Arthrographic studies in painful hemiplegic shoulders. Arch Phys Med Rehabil. 1984;65:254-256. [Medline] [Order article via Infotrieve]

17. Spaans F, Wilts G. Denervation due to lesions of the central nervous system: an EMG study in cases of cerebral contusion and cerebrovascular accidents. J Neurol Sci.. 1982;57:291-305. [Medline] [Order article via Infotrieve]

18. Benecke R, Berthold A, Conrad B. Denervation activity in the EMG of patients with upper motor neuron lesions: time course, local distribution and pathogenetic aspects. J Neurol. 1983;230:143-151. [Medline] [Order article via Infotrieve]

19. Zalis AW, Lafratta CW, Fauls LB, Oester YT. Electrophysiological studies in hemiplegia: lower motor neuron findings and correlates. Electromyogr Clin Neurophysiol.. 1976;16:151-162. [Medline] [Order article via Infotrieve]

20. Kingery WS, Date ES, Bocobo CR. The absence of brachial plexus injury in stroke. Am J Phys Med Rehabil. 1993;72:127-135. [Medline] [Order article via Infotrieve]

21. Bhala RP. Electromyographic evidence of lower motor neuron involvement in hemiplegics. Arch Phys Med Rehabil. 1969;50:632-637. [Medline] [Order article via Infotrieve]

22. Hooshmand H. Chronic Pain: Reflex Symphathetic Dystrophy Prevention and Management. Ann Arbor, Mich: CRC Press; 1993:35-55.

23. Wynn Parry CB. Pain in avulsion lesions of brachial plexus. Pain.. 1980;9:41-53. [Medline] [Order article via Infotrieve]

24. Myers SJ, Lovelace RE. The motor unit and muscle action potentials. In: Downey JA, Myers SJ, Gonzalez EG, Lieberman JS, eds. The Physiological Basis of Rehabilitation Medicine. 2nd ed. Boston, Mass: Butterworth-Heinemann; 1994:243-282.




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