The effects of electromyography-triggered electrical stimulation on shoulder subluxation,muscle activation,pain,and function in persons with stroke: A pilot study

Abstract

OBJECTIVES: The purpose of this study was to examine the effects of task-oriented electromyography-triggered stimulation for shoulder subluxation, muscle activation, pain and upper extremity function in hemiparetic stroke patients.

METHODS: Twenty participants with subacute hemiparetic stroke were recruited for this study and were randomly divided into two groups: experimental group (n = 10) and control group (n = 10). Subjects in the experimental group participated in task-oriented electromyography triggered stimulation for 30 minutes, five times a week for four weeks, whereas the control group received cyclic functional electrical stimulation for 30 minutes, five times a week for four weeks. Subjects in both groups received conventional physical therapy for four weeks (30 min/day, five times/week). Data collected included the degree of shoulder subluxation which had been confirmed by X-ray, muscle activation of the supraspinatus and posterior deltoid muscles by electromyography, pain by the Visual Analogue Scale (VAS), and hand function by the Fugl-Meyer Assessment (FMA) before and after the four week exercise period.

RESULTS: The results showed significant improvement in shoulder subluxation, muscle activation, and VAS results in the experimental group, compared with the control group(p < 0.05). FMA scores showed no significant differences between the two groups.

CONCLUSIONS: In conclusion, task-oriented electromyography-triggered stimulation improved shoulder subluxation, muscle activation, pain and upper extremity function. These results suggest that task-oriented electromyography-triggered stimulation is effective and beneficial for individuals with subacute stroke, and that further studies should be conducted on multivarious anatomical regions.

Keywords

Stroke subluxation task oriented exercise electromyography triggered stimulation

1 Introduction

Shoulder subluxation not only causes shoulder pain, but also has a significant effect on the process of rehabilitation treatment for stroke patients as a major factor impeding the upper extremity function (Faghri et al., 1994; Taketomi, 1975; Van Ouwenaller, Laplace, & Chantraine, 1986; Yu, Chae, Walker, & Fang, 2001).

As treatment modalities for prevention of shoulder subluxation and neurological recovery, use of sling, Functional Electrical Stimulation (FES), or muscle strengthening can be applied (Linn, Granat, & Lees, 1999). FES among them is a treatment method of promoting movements of the affected muscle, and is effective in aiding the recovery of muscle activation of shoulder muscles, which is an important factor in prevention of subluxation (Kobayashi, Onishi, Ihashi, Yagi, & Handa, 1999). After Basmajian and Bazant (1959) and Chaco and Wolf (1971) found that supraspinatus and posterior deltoid muscles affect shoulder subluxation, many studies have applied FES on these two muscles. Kobayashi et al. (1999) reported a reduced degree of subluxation and increased muscle activation when FES was applied on supraspinatus and deltoid muscles of stroke patients. A study by Yu et al. (2004) showed that FES was effective in reducing shoulder subluxation and pain. However, other researchers described that FES application had no direct change in the motor cortex area since it induced repetitive movements without cognitive judgment as it caused passive muscle contraction in the target muscle by steady electric currents (Kleim, Barbay, & Nudo, 1998; Plautz, Milliken, & Nudo, 2000).

Electromyography-triggered functional electrical stimulation (EMG-triggered FES) is a treatment method to induce self-regulatory, active muscle contraction as it is designed to initiate electrical stimulation upon muscle contraction over the set threshold (Francisco et al., 1998). Studies which compared the application of cyclic FES and EMG-triggered FES on stroke patients reported that EMG-triggered FES was more effective (de Kroon, Ijzerman, Chae, Lankhorst, & Zilvold, 2005; Bolton, Cauraugh, & Hausenblas, 2004). EMG-triggered FES can be used in task-oriented training in which tasks or activities that are related to daily life are repeatedly trained (Francisco et al., 1998), and task-oriented training can be a useful therapeutic intervention for functional recovery since it easily induces functional movements by motivation (Blundell, Shepherd, Dean, Adams, & Cahill, 2003).

A recent study reported that patient’s voluntary movement training with EMG-triggered FES was an effective intervention for the recovery of upper extremity movement (Mangold, Schuster, Keller, Zimmermann-Schlatter, & Ettlin, 2009), and that it is more effective than FES in subacute stroke patients (de Kroon et al., 2005). However, most studies applied EMG-triggered FES on the distal part of the upper extremity, and studies on shoulder subluxation mostly investigated the effect of cyclic FES in acute or chronic stroke patients. Therefore, this study aimed to investigate the effects of EMG-triggered FES applied with tasks on shoulder subluxation, muscle activation, pain, and function of the upper extremity in subacute stroke patients with shoulder subluxation.

2 Methods

2.1 Participants

This study was conducted in 20 adult stroke in patients with shoulder subluxation at I Hospital, and subjects who signed on the consent form for participation were selected after providing sufficient explanations on the entire objective and process of the study. The inclusion criteria for subjects were as follows:

1) had no pathological disease in the shoulder joint before the onset, 2) has shoulder subluxation of 9.5 mm or greater (Hall, Dudgeon, & Guthrie, 1995), 3) diagnosed with stroke and has the MMT Grade 2 or higher, 4) less than 6 months from the onset, 5) has Mini-Mental Status Examination (MMSE) score of 21 or higher, 6) has no cardiac pacemaker or metal transplant, 7) understands the objective of this study and consents to participate in the study, 8) is not participating in an experiment similar to this study (Table 1).

This study was approved by the Institutional Review Board of Sahmyook University, and all subjects signed the consent form prior to participation.

2.2 Protocol

This study was a pilot randomized controlled trial (RCT) design. To minimize selection bias, subjects were randomly divided into the experimental group (n = 10) and the control group (n = 10). For randomization, a numbered stick (either 1 or 2) was picked out from a sealed envelope for each participant. For all subjects, evaluations on the degree of subluxation, muscle activation, pain, and function of the upper extremity were conducted before and after the training (Fig. 1 - flow chart). Both the training group and the control group participated in patient-specific conventional exercise program for the same amount of time. Stretching and strengthening exercise were consisted in the conventional exercise program. To compare the training effects on shoulder subluxation, X-ray, EMG, VAS, and Fugl-Meyer were used for measurements before and after the training. The assessments for the study were conducted by a physical therapist, an occupational therapist, and a radiology technologist, who understood the experiment and were skillful in manipulating the assessment tools. For single-blinding, none of them participated in the training.

2.3 Intervention

For the experimental group, EMG-triggered FES was conducted with tasks for 30 minutes a day, 5 times a week while only FES was conducted for 30 minutes a day, 5 times a week for the control group (4 weeks). Conventional physical therapy was conducted for 30 minutes a day, 5 times a week for both groups.

EMG-FES 1000 (Cyber Medic) was used for EMG-triggered electrical stimulation. Initially, patients sat on a chair with no arm rest and had their upper extremity comfortably hang downward. The experimental group was instructed to conduct two task-oriented exercises (to touch a stationary air ball with elbow, push a button with elbow), which included shoulder abduction and extension of the affected side, while EMG-triggered FES was applied simultaneously. FES electrodes were attached to supraspinatus and posterior deltoid (Baker & Parker, 1986; Faghri et al., 1994; Kobayashiet al., 1999; Linn et al., 1999; Wang, Chan, & Tsai, 2000) (Table 2).

The threshold for electric stimulation was set according to the maximum contraction intensity of each patient. Symmetric biphasic pulse was set at 35 Hz, single pulse of 200 μs, phase duration of 10 seconds, rest period of 10 seconds, ramp up of 5 seconds, and ramp down of 5 seconds. The stimulation intensity ranged between 10∼30 mA, in which each patient’s sufficient muscle contraction was observed and applied accordingly (von Lewinski et al., 2009).

2.4 Outcome measures

The degree of shoulder subluxation was measured by X-rays, which imaged the anterior-posterior view of the patient’s shoulder. Patients were seated and instructed to drop their arms downward in relaxation for the measurement of the vertical distance (d) between the inferior border of acromion and the superior aspect of humeral head in the photo (Zorowitz et al., 1995). X-rays and measurements were conducted by one radiologist before and after the training.

Surface EMG (Telemyo 2400 G2 Telemetry EMG system, Noraxon, U.S.A., 2007) was used to measure the muscle activation of supraspinatus and posterior deltoid. The sampling rate of electromyographic signals was set at 1500 Hz, and the frequency bandwidth was at 10∼450 Hz. Before placing the electrodes on the skin, hair was removed and the area of attachment was cleaned with alcohol to minimize skin resistance. The electrode for supraspinatus was attached on suprascapular fossa area, 2 cm above the center of the spine of scapula, and the electrode for posterior deltoid was obliquely attached to lateral angle 2 cm below the spine of scapula, parallel to the muscle fibers (Cram, Kasman, & Holtz, 1998). EMG signals were processed using the Myoresearch XP Master edition software (Noraxon Inc., Arizona, USA). RMS (root mean square) value was obtained after processing the measured signals with full wave rectification, and processed with the integrated EMG (I-EMG) value. To measure muscle activation of supraspinatus and posterior deltoid, isometric submaximum shoulder abductions and external rotations were conducted for 5 seconds each. This measurement was repeated for 3 times, and the mid 3 seconds of the 5-second contraction were used for analysis (Kobayashi et al., 1999).

VAS is a rating scale showing the degree of pain by the patient across the 10 cm straight line with “ 0 cm” for no pain, and “10 cm” for most severe pain. This scale is a measurement showing high reproducibility in expression of the degree of pain by the subject, and is the most widely used method to assess the pain intensity with reliability r = 0.76∼0.84 (Boonstra, De Waal Malefijt, & Verdonschot, 2008). Subjective level of pain was measured before and after training; for the measurement a therapist manually abducted and externally rotated the affected upper extremity of each patient (Ikai, Tei, Yoshida, Miyano, & Yonemoto, 1998).

The Fugl-Meyer Assessment-Upper Extremity, the most frequently used evaluation of impairment in the upper extremity, includes 33 items of motions in the proximal part and distal part of the upper extremity. According to the degree of execution of a movement, 0∼2 points are given, in the range of 0∼66, indicating that the higher the score is, the better the function is. High reliability was observed with the within-measurer reliability as r = 0.99, and with the between-measurer reliability as 0.94 (Duncan, Propst, & Nelson, 1983).

2.5 Data analysis

The normality of variables was assessed using the Shapiro-Wilk test. Independent t-test (for continuous variables) and the chi-square test (for categorical variables) were used for comparison of the baseline characteristics of subjects in the experimental and control groups. Paired t-test was used for within-group comparison and independent t-test was used for between-group comparison. The level of statistical significance was set at 0.05. SPSS 12.0 (SPSS Inc.) was used for statistical analysis.

3 Results

The mean change value of subluxation before and after training were 4.95±5.29 cm in the experimental group, and were 0.50±2.47 cm in the control group, which showed a significant improvement in the degree of shoulder subluxation in the experimental group compared to the control group. Muscle activation of supraspinatus and posterior deltoid in the experimental group showed a significant improvement (mean change value of 77.91±87.14, 54.24±62.41 mV*S) than the control group (16.05±28.58, 1.21±24.57 mV*S), and pain was also significantly improved with external rotation in the experimental group (1.90±2.08, 1.60±1.71 points on VAS) with no significant change in the control group before and after training (0.30±2.54, 0.20±2.04 points on VAS). The total score of the Fugl-Meyer Assessment showed no significant between-group difference, but the subscales on shoulder (shoulder flexion, retraction, abduction, external rotation) showed significant improvement in the experimental group than in the control group (p < 0.05) (Fig. 2).

4 Discussion

This study compared the effects of task-combined EMG-triggered FES and common FES on the degree of subluxation, muscle activation, pain, and function of the upper extremity in early stroke patients. There was a significant improvement in the degree of subluxation, muscle activation, and pain in the experimental group compared to the control group after training.

Kobayashi et al. (1999) examined the activation of shoulder abductors after applying FES for 6 weeks in shoulder subluxation patients, and found a significant increase in muscle activation of supraspinatus and deltoid. This showed that electrical stimulation helped maintain and recover muscle activation by inducing active contraction of the affected muscle by stimulating the motor nerves. subject who were able to actively contract the muscles. The results in this study showed a significant increase in the degree of muscle activation in supraspinatus and posterior deltoid after application of task-oriented EMG-triggered FES compared to common FES application. This result is considered to be due to active muscle contraction needed in EMG-triggered FES. Movement is caused by an electrical stimulation which stimulates the proprioceptive feedback that returns to the somatosensory cortex, completing the sensorimotor circuit (Nudo, 1999). Thus, task-oriented EMG-triggered FES is more effective in motor learning than the common FES voluntary movement and proprioceptive input are involved in the beginning of a movement.

Faghri et al. (1994) applied FES on the affected shoulders for 6 weeks, and reported a significant decrease in subluxation by presenting the results of measurement changes in subluxation degrees on X-ray, and Baker and Parker (1986) reported that there was a significant decrease in subluxation in the group treated with FES compared to the group with common physical therapy only.

In this study, task-oriented EMG-triggered FES was found to be more effective for reduction of subluxation than common FES. Such result is considered to be based on the recovery of supraspinatus and posterior deltoid muscle power, which is reported to have an impact on shoulder subluxation and shoulder girdle stabilization (Baker & Parker, 1986).

The degree of pain in shoulder abduction and external rotation was also evaluated in this study. After training, pain was significantly decreased in the experimental group compared to the control group. This result is supported by a study by Kobayashi et al. (1999), which reported that a decrease in shoulder pain by FES had a larger correlation with the degree of increase in muscle activation than the degree of reduction in shoulder subluxation, and that FES had direct impact on pain control, but there was a difference depending on the experiment period and intensity.

In this study, the Fugl-Meyer Assessment for Upper Extremity was conducted as an independent functional assessment after training. No significant between-group difference was found in upper extremity function scores. According to Hedman, Sullivan, Hilliard, and Brown (2007), it was rather difficult to measure a change after shoulder-focused experiment, because the shoulder motions could not be accurately assessed only by the Fugl-Meyer Assessment for Upper Extremity. The results of shoulder flexion, retraction, abduction, and external rotation items in the Fugl-Meyer upper extremity function assessment each showed a significant change in the upper extremity function in the experimental group than the control group. However in the future, it would be necessary to apply an accurate assessment tool for the measurement of functional recovery in the shoulder in order to accurately compare the therapeutic effect between groups.

This study found positive effects of task-oriented EMG-triggered FES on shoulder subluxation, muscle activation, and pain in subacute stroke patients. However, it is difficult to generalize the results because of the study’s small number of subjects, and because only two types of task-oriented exercises were tested in this study. Therefore, it is necessary to develop more various types of tasks for the treatment of shoulder subluxation to be applied with EMG-triggered FES in larger number of subjects.

Conflict of interest

The authors declare that there were no conflicts of interest.

Footnotes

Acknowledgments

This study was supported by the research grant of Gachon University.

References

Baker

L. L.

, & Parker

(1986). Neuromuscular electrical stimulation of the muscles surrounding the shoulder. Phys Ther 66(12), 1930–1937.

Basmajian

J. V.

, & Bazant

F. J.

(1959). Factors preventing downward dislocation of the adducted shoulder joint. An electromyographic and morphological study. J Bone Joint Surg Am 41, 1182–1186.

Blundell

S. W.

, Shepherd

R. B.

, Dean

C. M.

, Adams

R. D.

, & Cahill

B. M.

(2003). Functional strength training in cerebral palsy: A pilot study of a group circuit training class for children aged 4-8 years. Clin Rehabil 17(1), 48–57.

Bolton

D. A.

, Cauraugh

J. H.

, & Hausenblas

H. A.

(2004). Electromyogram-triggered neuromuscular stimulation and stroke motor recovery of arm/hand functions: A meta-analysis. J Neurol Sci 223(2), 121–127.

Boonstra

M. C.

, De Waal Malefijt

M. C.

, & Verdonschot

(2008). How to quantify knee function after total knee arthroplasty? Knee 15(5), 390–395.

Chaco

, & Wolf

(1971). Subluxation of the glenohumeral joint in hemiplegia. Am J Phys Med 50(3), 139–143.

Cram

J. R.

, Kasman

G. S.

, & Holtz

(1998). Introduction to surface electromyography. Gaithersburg, Md.: Aspen Publishers.

de Kroon

J. R.

, Ijzerman

M. J.

, Chae

, Lankhorst

G. J.

, & Zilvold

(2005). Relation between stimulation characteristics and clinical outcome in studies using electrical stimulation to improve motor control of the upper extremity in stroke. J Rehabil Med 37(2), 65–74.

Duncan

P. W.

, Propst

, & Nelson

S. G.

(1983). Reliability of the Fugl-Meyer assessment of sensorimotor recovery following cerebrovascular accident. Phys Ther 63(10), 1606–1610.

10.

Faghri

P. D.

, Rodgers

M. M.

, Glaser

R. M.

, Bors

J. G.

, Ho

, & Akuthota

(1994). The effects of functional electrical stimulation on shoulder subluxation, arm function recovery, and shoulder pain in hemiplegic stroke patients. Arch Phys Med Rehabil 75(1), 73–79.

11.

Francisco

, Chae

, Chawla

, Kirshblum

, Zorowitz

, Lewis

, et al. (1998). Electromyogram-triggered neuromuscular stimulation for improving the arm function of acute stroke survivors: A randomized pilot study. Arch Phys Med Rehabil 79(5), 570–575.

12.

Hall

, Dudgeon

, & Guthrie

(1995). Validity of clinical measures of shoulder subluxation in adults with poststroke hemiplegia. Am J Occup Ther 49(6), 526–533.

13.

Hedman

L. D.

, Sullivan

J. E.

, Hilliard

M. J.

, & Brown

D. M.

(2007). Neuromuscular electrical stimulation during task-oriented exercise improves arm function for an individual with proximal arm dysfunction after stroke. Am J Phys Med Rehabil 86(7), 592–596.

14.

Ikai

, Tei

, Yoshida

, Miyano

, & Yonemoto

(1998). Evaluation and treatment of shoulder subluxation in hemiplegia: Relationship between subluxation and pain. Am J Phys Med Rehabil 77(5), 421–426.

15.

Kleim

J. A.

, Barbay

, & Nudo

R. J.

(1998). Functional reorganization of the rat motor cortex following motor skill learning. J Neurophysiol 80(6), 3321–3325.

16.

Kobayashi

, Onishi

, Ihashi

, Yagi

, & Handa

(1999). Reduction in subluxation and improved muscle function of the hemiplegic shoulder joint after therapeutic electrical stimulation. J Electromyogr Kinesiol 9(5), 327–336.

17.

Linn

S. L.

, Granat

M. H.

, & Lees

K. R.

(1999). Prevention of shoulder subluxation after stroke with electrical stimulation. Stroke 30(5), 963–968.

18.

Mangold

, Schuster

, Keller

, Zimmermann-Schlatter

, & Ettlin

(2009). Motor training of upper extremity with functional electrical stimulation in early stroke rehabilitation. Neurorehabil Neural Repair 23(2), 184–190.

19.

Nudo

R. J.

(1999). Recovery after damage to motor cortical areas. Curr Opin Neurobiol 9(6), 740–747.

20.

Plautz

E. J.

, Milliken

G. W.

, & Nudo

R. J.

(2000). Effects of repetitive motor training on movement representations in adult squirrel monkeys: Role of use versus learning. Neurobiol Learn Mem 74(1), 27–55.

21.

Taketomi

(1975). Observations on subluxation of the shoulder joint in hemiplegia. Phys Ther 55(1), 39–40.

22.

Van Ouwenaller

, Laplace

P. M.

, & Chantraine

(1986). Painful shoulder in hemiplegia. Arch Phys Med Rehabil 67(1), 23–26.

23.

von Lewinski

, Hofer

, Kaus

, Merboldt

K. D.

, Rothkegel

, Schweizer

, et al. (2009). Efficacy of EMG-triggered electrical arm stimulation in chronic hemiparetic stroke patients. Restor Neurol Neurosci 27(3), 189–197.

24.

Wang

R. Y.

, Chan

R. C.

, & Tsai

M. W.

(2000). Functional electrical stimulation on chronic and acute hemiplegic shoulder subluxation. Am J Phys Med Rehabil 79(4), 385–390; quiz 391-384.

25.

D. T.

, Chae

, Walker

M. E.

, & Fang

Z. P.

(2001). Percutaneous intramuscular neuromuscular electric stimulation for the treatment of shoulder subluxation and pain in patients with chronic hemiplegia: A pilot study. Arch Phys Med Rehabil 82(1), 20–25.

26.

D. T.

, Chae

, Walker

M. E.

, Kirsteins

, Elovic

E. P.

, Flanagan

S. R.

, et al. (2004). Intramuscular neuromuscular electric stimulation for poststroke shoulder pain: A multicenter randomized clinical trial. Arch Phys Med Rehabil 85(5), 695–704.

27.

Zorowitz

R. D.

, Idank

, Ikai

, Hughes

M. B.

, & Johnston

M. V.

(1995). Shoulder subluxation after stroke: A comparison of four supports. Arch Phys Med Rehabil 76(8), 763–771.