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514

Top Stroke Rehabil 2012;19(5):514–522
© 2012 Thomas Land Publishers, Inc.
www.thomasland.com

doi: 10.1310/tscir1905-514

Top Stroke Rehabil 2012;19(6):514–522
© 2012 Thomas Land Publishers, Inc.
www.thomasland.com

doi: 10.1310/tsr1906-514

Evidence for Therapeutic Interventions 

for Hemiplegic Shoulder Pain During 

the Chronic Stage of Stroke: A Review

Ricardo Viana, MD,

1,2

 Shelialah Pereira, PT, MSc,

1,3

 Swati Mehta, MA,

1,3

 

Thomas Miller, MD, FRCPC, 

1,2,3

 and Robert Teasell MD, FRCPC

1,2,3

1

St. Joseph’s Health Care, Parkwood Hospital, London, Ontario; 

2

Department of Physical Medicine and Rehabilitation, Schulich School 

of Medicine and Dentistry, Western University, London, Ontario; 

3

Aging, Rehabilitation and Geriatric Care Program, Lawson Health 

Research Institute, London, Ontario, Canada

Objective: To determine the effectiveness of therapeutic interventions targeting hemiplegic shoulder pain (HSP) more 
than 6 months post stroke. Methods: A literature search of multiple databases (PubMed, CINAHL, Ovid, and EMBASE) 
was conducted to identify articles published in the English language from 1980 to April 2012. Studies were included if 
(1) all participants were adults who had sustained a stroke; (2) research design was a randomized controlled trial (RCT) 
that examined the effectiveness of any treatment for HSP; (3) all participants had experienced stroke at least 6 months 
previously; and (4) an assessment of pain had been conducted before and after treatment using a standardized method. 
The following data were extracted: patient characteristics (ie, age, gender, time since stroke), sample size, study design, 
measurement of pain pre and post treatment, and adverse events. Results: Ten RCTs (PEDro scores 4–9) met inclusion 
criteria and included a total sample size of 388 individuals with a mean age of 53.2 years (range, 43.6–73.2). Mean time 
post stroke was 18.4 months. Three studies addressed the use of botulinum toxin type A (BTx-A); 2 studies examined 
electrical stimulation; 3 studies focused on intraarticular glenohumeral corticosteroid injections; 1 studied subacromial 
corticosteroid injections; and 1 study looked at massage therapy. Conclusions: Positive outcomes were noted with the use 
of corticosteroid injections and electrical stimulation and confl icting results were seen regarding the use of BTx-A. Overall, 
these targeted therapies provide benefi t in the treatment of HSP in individuals who are more than 6 months post stroke. 
Key words: chronic strokehemiplegic shoulder pain

H

emiplegic shoulder pain (HSP) is a com-
mon complication post stroke, which 
may reduce participation in rehabilita-

tion activities, contribute to activity avoidance, 
and reduce quality of life.

1–5

 It is estimated that 

28% of individuals with HSP will develop symp-
toms within 2 weeks; by 4 months, up to 87% 
will be affected.

6

 Although the pain will resolve 

by 6 months in the majority of cases, at least 20% 
of patients experience persistent, often debili-
tating, symptoms.

6,7

 It is not clear whether this 

improvement is due to treatment or the natural 
history of the condition. The etiology of HSP is 
multifactorial. Mechanisms include structural 
injury from glenohumeral subluxation, capsular 
contractures, or rotator cuff pathology. Chronic 
HSP may develop over time and is thought to 
be due to treatment-resistant structural injury, 
abnormal posture of the hemiplegic shoulder 
that damages the surrounding tissues,

7

 or peri-

articular muscle spasticity.

2,4

With such a variety of possible etiologies, it is 

no surprise that interventions are equally varied. 
Current management includes physiotherapy, 
massage therapy, strapping, slings and other 
supports to minimize glenohumeral subluxation, 
intraarticular or subacromial corticosteroid 
injections, suprascapular ner ve blocks, 
percutaneous or superficial electrical muscle 
stimulation, and botulinum toxin type A (BTx-A) 
intramuscular injections.

8

 Early management 

focuses on prevention with proper positioning 
and range of motion activities or on treatment 
in the acute or subacute stages post stroke.

8

 This 

is expected given that most stroke survivors 
present with symptoms during this time. It is 
diffi cult to determine the treatment effect given 

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Therapeutic Interventions for Hemiplegic Shoulder Pain 

515

the methodological quality of many of the studies; 
however, the overall estimate of treatment effect 
for the available treatments has been reported 
at 30% to 50%

9

 for the poststroke population 

as a whole. This is likely due to the inconsistent 
defi nition of HSP

7,10–12

 or lack of an appropriate 

clinical examination as a guide for treatment 
modality selection. The objective of this review 
is to determine the effectiveness of interventions 
targeting HSP 

6 months post stroke and present 

them by modality for specifi c, possible etiologies.

Methods

Search strategy

A literature search was conducted in multiple 

databases (PubMed, Scopus, Ovid, and CINHAL) 
to identify relevant articles published from 1980 
to April 2012. Reference lists were also hand 
searched for additional articles that may not have 
been identifi ed during the original search.

Selection criteria

Studies were selected for inclusion if (1) all 

participants were adults (

18 years of age) who 

had sustained a stroke; (2) research design was a 
randomized controlled trial (RCT) that examined 
the effectiveness of any treatment for HSP; (3) all 
subjects included in the study had experienced 
stroke at least 6 months previously; and (4) an 
assessment of pain had been conducted before 
and after treatment using a standardized method. 
Control conditions could include a placebo, 
active control, or no treatment depending on the 
treatment under investigation.

Commentaries, letters, abstracts, reviews/

guidelines, imaging studies, case studies or case 
series, non-human trials, and those articles that 
were not in English were excluded.

Study selection and assessment of methodological 
quality

The titles and abstracts of all the articles 

identifi ed in the literature search were screened 
for eligibility. Trials included for the review were 
assessed for methodological quality using the 

Physiotherapy Evidence Database (PEDro) scoring 
system.

13

 PEDro is a 10-item scale, which assesses 

the internal validity of a study where each item 
is awarded a score of yes (1) or no (0). The total 
scores range from 0 to 10. The strength of evidence 
was assessed using guidelines developed for the 
Evidence-Based Review of Stroke Rehabilitation

8

 

organizing the PEDro scores into the following 
categories: “excellent” quality, 9–10; “good” quality, 
6–8; “fair” quality, 4–5; and “poor” quality <4.

Results

Search results

A total of 226 articles were identifi ed  after 

removing duplicates. After reviewing titles and 
abstracts and hand screening reference lists, 
10 articles were included in the review.

14–23

 A 

description of the search results is presented in 
Figure 1.

Articles included studies evaluating the 

effectiveness of BTx-A,

14–16

 regarding superfi cial 

and percutaneous electrical stimulation,

17,18

 

and focusing on intraarticular glenohumeral 
corticosteroid injections,

19–21

 subacromial steroid 

injections,

22

 and massage therapy.

23

  Table 1 

provides a detailed description of the studies 
divided into their respective treatment categories.

The total sample size was 388 participants, 

which was composed of 229 males and 159 females. 
The mean age of this pooled sample was 53.2 years 
(range, 43.6 –73.2), and the mean time post stroke 
was 18.4 months.

In most of the studies,

14–20,22

 participants received 

“conventional” physical therapy consisting of 
stretching and range of motion (ROM) exercises 
and neuromuscular facilitation. Rah

22

 was more 

prescriptive, allowing participation in therapy to 
start only 2 weeks post injection to minimize the 
risk of tendon rupture. These participants received 
a graduated return to therapy program starting 
2 to 4 weeks post injection. In 2 studies,

21,23

 no 

details were reported regarding additional therapy. 
One study

17

 reported that a proportion of the 

study participants received oral analgesia but did 
not report the class, timing, frequency, or dose of 
use. They did report that these participants were 
equally represented in the treatment and control 

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Figure 1.  Flow chart depicting results of the literature search.

Search Results (minus duplicates)= 225

(PubMed n=28, Ovid n=77, Scopus n=96, CINAHL n=24)

Articles not relevant to current
review = 216

Reviews (31)

Imaging study (18)

Case studies (20)

Case series (2)

Published abstracts (3)

<6 months post stroke (22)

Etiology studies (20)

Prevalence studies (36)

Treatment of arm function (30)

Guidelines (2)

Not English (3)

Pain assessment (22)

Time post stroke not indicated (1)

No outcomes reported (1)

Mixed time post stroke (4)

Study protocol (1)

Botulinum

toxin

(3)

Electrical

stimulation

(2)

Steroid

injection

(4)

Included in the review = 10

Articles identified by hand

searching references = 1

Active

therapies

(1)

groups, and no changes were made to the dose or 
regimens during the study period.

Adverse events were reported by 4 studies

15–17,22

 

impacting a total of 25 participants (6.4% of total 

sample; 13 in the intervention groups and 12 in 
the control groups). Most were described as minor 
including pain

15,16

 or vasovagal syncope

16,22

 at 

the time of the intervention. The most signifi cant 

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Treatment categories

Botulinum toxin

Three studies used BTx-A. The PEDro 

scores ranged from 6 to 8 (good to excellent 
methodological quality). Two studies

14,16

 targeted 

event was reported by Chae

17

 where the tips of 

the percutaneous leads remained intramuscular in 
4 participants. These participants were followed 
for 18 months, and there was no associated 
infection or granulomatous reaction or associated 
pain or functional limitation.

Table 1.  Participant characteristics and study details

Study

PEDro

Country

No. of participants 

(M/F)

Time post 

stroke (months)

Intervention

Outcome 

measure

de Boer et al, 
 2008

14

6

Netherlands

21

(12/9)

  7.65

BTx-A (BOTOX) 100 U vs 
placebo
Injection into subscapularis

VAS (-)

Kong et al, 2007

15

8

China

16

(11/5)

9.3

BTx-A (Dysport ) 500 U vs 
placebo
Injection into pectoralis major 
and biceps brachii

VAS (-)

Yelnik et al, 
 2007

16

7

France

20

(15/5)

16.75

BTx-A (Dysport ) 500 U vs 
placebo
Injection into subscapularis

NPS (+)

Lakse et al, 
 2009

19

4

Turkey

38

(18/20)

12

Triamcinolone acetonide 
(40 mg) + prilocain 9 mL + 
TENS (20 min/d x 19 sessions) + 
PT vs control [TENS (20 min/d x 
19 sessions] + PT)

VAS (+)

Lim et al, 2008

20

9

South Korea

29

(15/14)

 8.85

Triamcinolone acetonide (40 mg) 
vs 100 U BTx-A (BOTOX)
•  

Group 1: BTx-A into 
infraspinatus, pectoralis 
& supscapularis, saline 
intraarticular

•  

Group 2: Saline into the 
muscles’ triamcinolone 
intraarticular

NPS (+/−)

Yasar et al, 2011

21

5

Turkey

26

(17/9)

 9.04

Triamcinolone acetonide 
(40 mg) intraarticular 
injection vs 10 mL 2% prilocain 
suprascapular nerve block

VAS(+/−)

Rah et al, 2012

22

5

Republic of 
Korea

58

(39/19)

21.2

Subacromial injection 
triamcinolone acetonide 
(40 mg) vs 5 mL 1% lidocaine

VAS (+)

Chae et al, 2005

17

7

USA

61

(36/25)

31.9

Intramuscular electrical 
stimulation to supraspinatus, 
posterior & middle deltoid, and 
upper trapezius (6 h/d x 6 wks) 
vs sling

NPS (+)

Kobayshi et al, 
 1999

18

5

Japan

17

(15/2)

28.77

Surface FES vs no FES
Target supraspinatus vs middle 
deltoid vs none

VAS (+)

Mok et al, 2004

23

5

Hong Kong

102

(51/51)

Slow stroke back massage vs no 
treatment
Massage provided for 10 min 
per night for 7 days

VAS (+)

Note: BTx-A = Botulinum toxin type A; d = day; FES = functional electrical stimulation; h = hour; NPS = Numeric Pain Scale; PT = physical 

therapy; TENS = transcutaneous electrical stimulation; VAS = Visual Analog Scale; W/C = wheelchair; wk = week.

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40 mg intraarticular injection of triamcinolone 
acetonide (TA). Follow-up was arranged for 2, 6, 
and 12 weeks post treatment. Pain scores (NPS) 
for both groups improved from baseline (BTx-A: 
7.9 ± 0.3 to 3.2 ± 0.5; TA: 7.6 ± 0.5 to 5.2 ± 0.8, 
at 12 weeks); however, there was no statistically 
signifi cant difference between groups (P = .064). 
Yaser et al

21

 compared an intraarticular injection 

of 40 mg TA to a suprascapular nerve block using 
10 mL of 2% prilocain. Follow-up measures 
were arranged for 1 hour, 1 week, and 1 month 
post treatment. Pain score (VAS) was similar 
between groups (P > .05). Although the authors 
provided baseline scores, they did not provide 
follow-up scores for each of the time points. One 
study looked at subacromial injections in the 
treatment of HSP 

6 months post stroke. Rah et 

al

22

 compared a subacromial injection of 40 mg TA 

to 5 mL of 2% lidocaine. Follow-up was arranged 
for 2, 4, and 8 weeks post treatment. Pain score 
(VAS) improvement was signifi cantly greater in 
the corticosteroid group for daytime pain at 4 and 
8 weeks (P = .048 and P = .004, respectively) and 
for night time pain at 2, 4, and 8 weeks (P = .004, 
P = .004, P < .001, respectively).

Electrical stimulation

Two studies addressed the use of neuromuscular 

electrical stimulation. One study examined 
percutaneous stimulation and the other studied 
surface stimulation. PEDro scores were 5 and 7. 
Chae et al

17

 compared intramuscular electrical 

stimulation to the supraspinatus, posterior and 
middle deltoid, and upper trapezius musculature 
for 6 h/day for 6 weeks to use of a sling. Follow-up 
was arranged for 3, 6, and 12 months post 
treatment. Maximum pain score for the previous 
week [Brief Pain Inventory question 12’s numeric 
pain scale (NPS)] improved to a signifi cantly 
greater extent in the treatment group [Stim: 
baseline 7.59 ± 2.12 to 

Δ

 3 months 4.44 (3.68), 

Δ

 6 months 4.44 (3.56), 

Δ

 12 months 5.0 (3.3) vs 

Control: baseline 6.52 ± 2.29 to 

Δ

 3 months 0.68 

(1.85), 

Δ

 6 months 1.38 (2.81), 

Δ

 12 months 2.31 

(3.21);  P < .001, at all time points]. Kobayshi et 
al

18

 randomly assigned 17 participants to surface 

stimulation of supraspinatus muscle (group 1) 
versus surface stimulation of the middle deltoid 

the subscapularis muscle. de Boer et al

14

 injected a 

total of 100 U (BOTOX) to 2 sites in the subscapularis 
muscle at a 2:1 dilution. Pain, measured by the 
visual analog scale (VAS), showed no signifi cant 
difference with respect to control at 12 weeks 
[BTx-A: 44.9 mm (15.2 mm) to 38.1 mm (18.2 
mm) vs Control: 61.7 mm (23.2 mm) to 46.8 mm 
(27.2 mm); P = .81]. Yelnik et al

16

 injected a total 

of 500 U (Dysport), of unknown dilution, targeting 
the motor endplates using electrical stimulation. 
The control group was injected with all the 
constituents of Dysport solvent but no BTx-A, and 
follow-up was performed at 1, 2, and 4 weeks. Pain 
score, measured by the numeric pain scale (NPS), 
showed a signifi cant improvement with respect to 
control at 4 weeks post injection (BTx-A: 7.5 to 1.5 
vs Control: 5.5 to 4; P = .025). One study targeted 
the pectoralis major muscle. Kong et al

15

 injected a 

total of 500 U (Dysport) diluted in 2.5 mL of saline 
with 250 U to pectoralis major and 250 U to biceps 
brachii. The control group received intramuscular 
injection of normal saline, and participants were 
followed up at 4, 8, and 12 weeks. Pain score (VAS) 
showed no signifi cant improvement with respect to 
pain control at 1, 2, and 3 months (P = .21, P = .48, 
and P = .5, respectively).

Corticosteroid injection therapy

Three studies investigated intra-articular 

corticosteroid injections. PEDro scores ranged 
from 4 to 9. Lakse et al

19

 compared 40 mg 

of intraarticular triamcinolone acetonide and 
9 mL of prilocain with transcutaneous electrical 
stimulation (TENS) for 20 minutes per day for 
19 days and physical therapy (PT) versus TENS 
and PT alone. Follow-up was arranged at 1 and 
4 weeks. Pain scores (VAS) were signifi cantly 
improved in the injection group at time points at 
rest, during activity, and at night (week 1: P = .01, 
P = .02, P = .00; week 4: P = .03, P = .03, P = .01) 
when compared to the control group during these 
activities. Lim et al

20

 compared intra-articular 

triamcinolone acetonide to intramuscular BTx-
A. One group received a total of 100 U of BTx-A 
(BOTOX) at a 4:1 dilution into infraspinatus, 
pectoralis major, and subscapularis muscles and 
an intraarticular injection of saline; the other group 
received intramuscular injections of saline and a 

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and BTx-A into overactive, spastic, periarticular 
muscles. There were no RCTs examining the use 
of physical modalities, strapping or other shoulder 
support systems, or analgesic medication, 
specifi cally topical or oral agents including the 
use of opioids, in chronic HSP. As a whole, the 
treatments studied had a positive impact on HSP 
management in this population. Because each 
treatment targets a different, suspected, etiology, 
they will be initially discussed separately.

BTx-A is thought to decrease the activity of 

periarticular muscles leading to muscle relaxation 
and improved ROM. There are no studies 
to date demonstrating a correlation between 
muscle activity or spasticity and HSP, but a 
causal mechanism is inferred based on positive 
treatment responses. In this review, among the 
4 studies that examined the use of BTx-A, there 
were differences in target muscle (subscapularis 
vs pectoralis major), dose and type of BTX type A 
(BOTOX vs Dysport), and use of neuromuscular 
targeting (neuromuscular electrical stimulation vs 
anatomical landmarking). Two of the studies were 
considered to be positive and 2 were negative.

Even though all studies use a BTx-A product, 

there is some variability between brands on dose 
equivalence. de Boer

14

 and Lim

20

 use BOTOX, 

whereas the others used Dysport. Wohlfarth et al

24

 

recently determined the dose equivalence between 
Dysport and BOTOX was 2.3–2.5:1 respectively, 
when mixed in saline. To compare dosages 
between studies, we have used this conversion 
and reported treatment dose in unit equivalents of 
Dysport. The dosages used in the studies ranged 
from 250 to 500 U.

The 2 negative studies

14,15

 differed by target 

muscle (subscapularis vs pectoralis major) 
and were similar in the dose of BTx-A (250 U 
equivalents of Dysport), the use of a low dilution 
(2–2.5:1), and no neuromuscular guidance for 
needle placement. The positive studies

16,20

 differed 

by target muscles (subscapularis muscle vs 
subscapularis muscle + pectoralis major muscle + 
infraspinatus muscle); they also differed from 
each other and the negative studies in that one 
used guidance (neuromuscular junction electrical 
stimulation) and the other used a high dilution 
of 4:1. Both of these studies used higher doses 
(250 to 500 U equivalents of Dysport)

muscle (group 2) versus no surface stimulation 
(control). The therapeutic electrical stimulation 
(TES) protocol consisted of negative monophasic 
rectangular pulses at a frequency of 20 Hz and 
pulse duration of 0.3 ms for the stimulation. 
Total stimulation time was 15 seconds including 
3 seconds of rising time and 2 seconds of falling 
time repeating in a pattern of 15 seconds on and 
15 seconds off for 15 minutes twice a day for 
6 weeks. Follow-up was arranged for 6 weeks 
post treatment. The primary outcome in this 
study was to determine the amount reduction in 
shoulder subluxation post stimulation. Pain was 
a secondary outcome and present in only 6 of the 
17 participants (Group 1: 3; Group 2: 3; Control: 1). 
A 15 cm VAS was used to measure pain. At the 
conclusion of the study, there was a reduction 
in mean VAS scores in the 2 intervention groups 
(Group 1: 10.33 cm to 7.83 cm; Group 2: 8.93 cm 
to 4.8 cm) compared to control (6.3 cm to 6.5 cm).

Hands-on therapy

Only one study addressed the use of hands-on 

therapy. Mok et al

23

 compared the use of slow 

stroke back massage for 10 minutes per night 
for 7 days to a no-treatment control. Follow-up 
was arranged for 3 days after the last treatment. 
The authors found that the treatment group had 
a signifi cant reduction in pain during and after 
the treatments (P < .05) compared to control, as 
measured by the VAS.

Discussion

Ten RCTs representing 5 distinct treatment 

modalities were identifi ed in this review that 
examined the management of HSP in stroke 
survivors 

6 months post stroke. Chronic HSP 

is thought to differ from early onset HSP and 
is associated with treatment-resistant structural 
injury, abnormal posture of the hemiplegic 
shoulder (including chronic subluxation), or 
increased spasticity of periarticular muscles.

4

 The 

treatments studied in this population address these 
presumed etiologies with the use of corticosteroid 
injections (either intraarticular or subacromial), 
electrical stimulation of weak periarticular muscle 
to minimize subluxation in order to reduce pain, 

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volume injection. The targeted muscles were large, 
so the negative studies may not have used a high 
enough dose or dilution to get the desired effect 
given they did not use neuromuscular targeting.

Intraarticular corticosteroid injections are 

given primarily in the management of capsular 
or glenohumeral pathology, whereas subacromial 
injections are used to treat rotator cuff or bursal 
pathologies. In this review, we identifi ed 4 studies 
addressing the use of corticosteroid injections, 
specifi cally TA, with confl icting results. Lakse 
reported signifi cant improvement in pain control, 
whereas the other groups showed no difference 
between treatment groups. Intraarticular injections 
were no better than BTx-A and the mean decrease 
in pain score was in favor of BTx-A (P = .051), 
whereas intraarticular injections were found 
to be equal in effi cacy to suprascapular nerve 
blocks. Unfortunately, Yaser et al

21

 did not provide 

follow-up pain scores but instead presented 
the follow-up results as statistical differences in 
repeated measurements, so we cannot comment 
on whether there was a signifi cant change from 
baseline in either the intraarticular or suprascapular 
nerve block group. The single article addressing 
subacromial injections

22

 reported significantly 

greater improvement in pain control. In conclusion, 
corticosteroid injections show a trend toward 
improving HSP in stroke survivors who are 

6 months post stroke, and intraarticular injections 

appear as equally effective as BTx-A intramuscular 
injections and suprascapular nerve blocks.

Two studies

17,18

 addressed the use of 

neuromuscular stimulation in the management 
of HSP 

6 months post stroke. Device wear 

times for both regimens were extensive, requiring 
stimulation up to 6 hours per day for an average of 
6 weeks. The study by Chae

17

 was strongly in favor 

of percutaneous neuromuscular stimulation for 
the management of HSP as well as for treatment of 
glenohumeral subluxation. Kobayshi

18

 used surface 

neuromuscular stimulation in the management 
of shoulder subluxation and reported some 
benefi t on pain in a small sample of participants. 
In reviewing the available information, we can 
conclude that the current state of the evidence in 
the use of surface neuromuscular stimulation in 
the management of HSP 

6 months post stroke 

is modest at best.

All studies differed by the dilution of BTx-A used. 

de Boer

14

 used a 2:1 dilution, Kong

15

 used 2.5:1, 

and Lim

20

 use 4:1. Yelnik’s study

16

 did not report 

the dilution used, so its impact on the positive 
outcome is unknown. Dilution can impact the 
effectiveness of BTx-A intramuscular injections. A 
recent study by Gracies et al

25

 explored the impact 

of dilution in neuromuscular treatment of the 
biceps brachii. In this study, one group received 
100 U of BTx-A at 1:1 dilution targeted to the 
neuromuscular junctions across 4 sites, a second 
group received 100 U of BTx-A at 1:1 dilution over 
4 sites away from the neuromuscular junctions, 
and a third group received 100 U of BTx-A at 5:1 
dilution over 4 sites away from the neuromuscular 
junctions. At the conclusion of the study, it was 
determined that low volume/low dilution targeted 
injections were as effective as high volume/high 
dilution nontargeted injections, and both are 
superior to low volume/low dilution nontargeted 
injections. This conclusion is supported by the 
fi nding that BTx-A diffuses in tissues and across 
tissue plains as far as 4.5 cm with dilutions of 
3:1 to 5:1.

26

 So at higher dilution, the BTx-A is 

able to more easily diffuse to and act on the target 
neuromuscular junctions, even if injected as far as 
4 to 4.5 cm away. Dilution appears to be associated 
with likelihood of pain relief in the studies included 
in this analysis, as the de Boer

14

 and Kong

15

 

studies used low dose, low dilution, nontargeted 
injections with negative results; Yelnik

16

 used high 

dose, targeted injections with positive impact on 
pain control; and Lim

20

 used low dose and high 

dilution and noted considerable change from 
baseline. Adjusting dose and dilution is patient- 
and clinician-specifi c, so no recommendation can 
yet be made on standard formulations.

Both the pectoralis major and subscapularis 

muscles were targeted in these studies. There are 
a number of variables impacting on the outcome 
of these studies, so a defi nitive  recommendation 
as to which muscle to target is not possible. 
Also, no studies have identifi ed a correlation 
between quantitative activity measured on 
electromyography (EMG) in these muscles and the 
incidence or intensity of HSP.

Only the Yelnik

16

 study used neuromuscular 

targeting. As we have learned from Gracies,

25

 lack 

of targeting may be overcome by high dilution, high 

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Therapeutic Interventions for Hemiplegic Shoulder Pain 

521

spasticity and the presence or intensity of HSP, as well 
as clearer recommendations regarding target muscle, 
dose, and dilution of BTx-A and the importance of 
neuromuscular targeting. Corticosteroid injections 
into the joint or subacromial space appear to be 
a good treatment option for HSP 

6 months post 

stroke. Electrical stimulation can be considered 
in individuals with HSP and glenohumeral 
subluxation, as it will improve the degree of 
subluxation and may help in pain control. There 
is no information available regarding the impact 
of shoulder support systems and/or the utility of 
oral analgesia, including opioids. More research 
is needed to more completely understand HSP 
and determine which modality, or combination of 
modalities, can best manage HSP 

6 months post 

stroke.

Acknowledgments

We would like to acknowledge funding from the 

Canadian Stroke Network.

Financial disclosure: We certify that no party 

having a direct interest in the results of the research 
supporting this article has or will confer a benefi t on us 
or on any organization with which we are associated 
and, if applicable, we certify that all fi nancial  and 
material support for this research (eg, NIH or NHS 
grants) and work are clearly identifi ed.

Mok et al

23

 studied the use of slow stroke back 

massage. The study follow-up was limited to 
3 days after the last treatment, so the authors were 
unable to determine whether the improvement in 
pain was lasting. Also, there was no blinding of the 
intervention, which carries a signifi cant bias. The 
available information points to limited evidence in 
support of slow stroke back massage as an option 
for pain control at the time of treatment, but 
more research must be performed to determine 
the persistence of the effect and whether there is 
a number of treatments, or “dose,” that would be 
needed to result in a lasting impact on pain control.

Conclusion

HSP is a prevalent and debilitating poststroke 

complication contributing to impairment and 
disability. The etiology of HSP is multifactorial; 
chronic HSP is thought to be secondary to treatment-
resistant structural injury, abnormal posturing 
or chronic shoulder subluxation, or increased 
periarticular muscle spasticity. Treatments directed 
toward these specifi c etiologies have demonstrated a 
positive impact on pain control in this population. 
More research is needed regarding the use of 
BTx-A in order to improve its effi cacy. Specifi cally, 
there needs to be a clearer understanding of the 
relationship between quantitative muscle activity or 

REFERENCES

1. Lindgren I, Jonsson AC, Norrving B, Lindgren 

A. Shoulder pain after stroke, a prospective 
population-based study. Stroke. 2007;38:
343–348.

2. Koog YH, Jin SS, Yoon K, BI Min BI. Interventions 

for hemiplegic shoulder pain: systematic review 
of randomized control trials. Disabil Rehabil. 
2010;32:282–291.

3. Turner-Stokes L, Jackson D. Shoulder pain after 

stroke: a review of the evidence base to inform the 
development of an integrated care pathway. Clin 
Rehabil.
 2002;16:276–298.

4. Black-Schaffer RM, Kirsteins AE, Harvey RL. 

Stroke rehabilitation. 2. Co-morbidities and 
complications.  Am Acad Phys Med Rehabil. 
1999;80:S8–S16.

5.  Gamble GE, Barberan E, Bowsher D, Tyrrell PJ, Jones 

AK. Post stroke shoulder pain: more common than 
previously realized. Eur J Pain. 2000;4:313–315.

6.  Gamble GE, Barberan E, Laasch HU, Bowsher D, Tyrrell 

PJ, Jones AK. Poststroke 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;6:467–474.

7. Kalichman L, Ratmansky M. Underlying pathology 

and associated factors of hemiplegic shoulder 
pain. Am J Phys Med Rehabil. 2011;90:768–780.

8. Teasell R, Foley N, Salter K, et al. Evidence-Based 

Review of Stroke Rehabilitation. 14th ed. 2011. 
wwwEBRSRcom.

9. Snels IAK, Dekker JHM, van der Lee JH, Lankhorst 

GJ, Beckerman H, Bouter LM. Treating patients 
with hemiplegic shoulder pain. Am J Phys Med 
Rehabil.
 2002;81:150–160.

10. Ratnasabapathy Y, Broad J, Baskett J, Pledger M, 

Marshall J, Bonita R. Shoulder pain in people with 
a stroke: a population-based study. Clin Rehabil. 
2003;17:304–311.

background image

522 T

OPICS

 

IN

 S

TROKE

 R

EHABILITATION

/N

OV

-D

EC

 2012

19. Lakse E, Gunduz B, Erhan B, Celik EC. The 

effect of local injections in hemiplegic shoulder 
pain: a prospective, randomized, controlled study. 
Am J Phys Med Rehabil. 2009;88:805-811; quiz 
12–14, 51.

20. Lim JY, Koh JH, Paik NJ. Intramuscular botulinum 

toxin-A reduces hemiplegic shoulder pain: a 
randomized, double-blind, comparative study 
versus intraarticular triamcinolone acetonide. 
Stroke. 2008;39:126–131.

21. Yasar E, Vural D, Safaz I, et al. Which treatment 

approach is better for hemiplegic shoulder 
pain in stroke patients: intra-articular steroid 
or suprascapular nerve block? A randomized 
controlled trial. Clin Rehabil. 2011;25:60–68.

22. Rah UW, Yoon SH, Moon do J, et al. Subacromial 

corticosteroid injection on poststroke hemiplegic 
shoulder pain: a randomized, triple-blind, 
placebo-controlled trial. Arch Phys Med Rehabil. 
2012;93:949–956.

23. Mok E, Woo CP. The effects of slow-stroke back 

massage on anxiety and shoulder pain in elderly 
stroke patients. Complement Ther Nurs Midwifery. 
2004;10:209–216.

24. Wohlfarth K, Sycha T, Ranoux D, Naver H, 

Caird D. Dose equivalence of two commercial 
preparations of botulinum neurotoxin type A: 
Time for a reassessment? Curr Med Res Opin. 
2009;25:1573–1584.

25. Gracies JM, Lugassy M, Weisz DJ, Vecchio M, 

Flanagan S, Simpson DM. Botulinum toxin dilution 
and endplate targeting in spasticity: a double-
blind controlled study. Arch Phys Med Rehabil. 
2009;90:9–16 e2.

26. Lim EC, Seet RC. Botulinum toxin: description 

of injection techniques and examination of 
controversies surrounding toxin diffusion. Acta 
Neurol Scand.
 2008;117:73–84.

11.  Zorowitz RD, Hughes MB, Idank D, Ikai T, Johnston 

MV. Shoulder pain and subluxation after stroke: 
Correlation or coincidence? Am J Occup Ther. 
1996;50:194–201.

12. Bohannon RW, Larkin PA, Smith MB, Horton MG. 

Shoulder pain in hemiplegia: statistical relationship 
with five variables. Arch Phys Med Rehabil. 
1986;67:514–516.

13. Moseley AM, Herbert RD, Sherrington C, Maher 

CG. Evidence for physiotherapy practice: a survey 
of the Physiotherapy Evidence Database (PEDro). 
Aust J Physiother. 2002;48:43–49.

14. de  Boer KS, Arwert HJ, de Groot JH, Meskers 

CG, Mishre AD, Arendzen JH. Shoulder pain and 
external rotation in spastic hemiplegia do not 
improve by injection of botulinum toxin A into the 
subscapular muscle. J Neurol Neurosurg Psychiatry. 
2008;79:581–583.

15. Kong KH, Neo JJ, Chua KS. A randomized 

controlled study of botulinum toxin A in the 
treatment of hemiplegic shoulder pain associated 
with spasticity. Clin Rehabil. 2007;21:28–35.

16. Yelnik AP, Colle FM, Bonan IV, Vicaut E. Treatment 

of shoulder pain in spastic hemiplegia by 
reducing spasticity of the subscapular muscle: a 
randomised, double blind, placebo controlled 
study of botulinum toxin A. J Neurol Neurosurg 
Psychiatry.
 2007;78:845–848.

17. Chae J, Yu DT, Walker ME, et al. Intramuscular 

electrical stimulation for hemiplegic shoulder 
pain: a 12-month follow-up of a multiple-center, 
randomized clinical trial. Am J Phys Med Rehabil. 
2005;84:832–842.

18. Kobayashi H, Onishi H, Ihashi K, Yagi R, Handa Y. 

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

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