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Current evidence in the management of poststroke hemiplegic shoulder pain: a review.

ABSTRACT

Hemiplegic shoulder pain is a common, complex, and distressing complication, which is related to stroke and occurs in the paralytic side of the patient. It not only presents in the early stage but also can persist into the chronic stage of stroke. The incidence of this complication varies from 12% to 58%, and the most common period of occurrence is at 8-10 weeks poststroke. The multifactorial etiology and underlying mechanisms make it intractable. It is difficult to get a clear description of the percentage of patients receiving adequate pain relief because of a large number of treatments and different results found in interventional studies performed in subjects in different stages of stroke. This review summarizes the incidence, temporal presentation, and etiology of hemiplegic shoulder pain and the current advances in its management and analyzes the reliability and validity of the studies. It suggests careful and regular assessment, and an integrated care model is necessary in practice.

Keywords: Assessment, hemiplegic shoulder pain, intervention, nursing, stroke

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According to the World Health Organization, 15 million people experience stroke worldwide each year. Of these, 5 million die, and another 5 million are permanently disabled. Europe averages approximately 650,000 stroke deaths each year (The Internet Stroke Center, 2013). Approximately 795,000 cases of stroke occur in the United States each year, making it the fourth leading cause of mortality in the United States when considered separately from other cardiovascular diseases. Stroke is the leading cause of serious, long-term disability in the United States and worldwide (American Heart Association, 2013). An estimated 1.5-2 million new strokes occur each year in mainland China. The official statistics data from 31 regions in 2005 showed that stroke was the second most common cause of death among both urban and rural residents of China (Liu et al., 2007). Many surviving patients have persistent disability. These deficits include mental and/or physical consequences of stroke, which influence the quality of life (QOL). Hemiplegic shoulder pain (HSP) is one of the common complications in people who are recovering from stroke. During a 1 -year period, a prospective population-based study including 416 first-ever patients with stroke reported that almost one third of the 327 patients who were followed up developed shoulder pain after stroke onset, most of them with moderate-to-severe pain (Lindgren, Jonsson, Norrving, & Lindgren, 2007). In a recent review conducted by Koog, Jin, Yoon, and Min (2010), HSP occurrence varied from 16% to 84%. The variable incident rates of HSP reported in these and other studies is likely because of differences in inclusion criteria and measurement approaches. Although these studies highlight the frequency of this complication for stroke survivors, additional evidence shows that these numbers may be low because of underreporting. A study performed in New Zealand confirmed the association between left-sided hemiplegia and increased risk for shoulder pain. The proportion of patients with stroke affecting the left side reporting ipsilateral shoulder pain varies over time from 10% at 1 week to 14% at 1 month and 20% at 6 months. The patients with right-sided hemiplegic stroke experiencing ipsilateral shoulder pain reported 12%, 13%, and 16% at the same time points, respectively. One possible interpretation of the result is that dysphasia associated with right-sided hemiparesis may lead to underreporting on that side (Ratnasabapathy et al., 2003).

HSP negatively affects the use of the affected limb, compromises functional recovery, and delays discharge from hospital or a rehabilitation center (Van Til, Renzenbrink, Groothuis, & Ijzerman, 2006). One hundred eighty-seven consecutive patients with stroke were divided into two groups, one composed of patients with HSP and the other composed of patients without HSP. The group without HSP showed significantly more improvement than the group with HSP in functional outcomes (t = -3.70, p = .01), and the hospitalization period was significantly shorter (p = .01; Barlak, Unsal, Kaya, Sahin-Onat, & Ozel, 2009). A cross-sectional study, including 61 chronic stroke survivors, confirmed the association and found HSP-reduced QOL (Chae et al., 2007a). The purpose of this article is to review the incidence and temporal presentation, etiology, and outcomes of HSP. Finally, updated management strategies focused on improvement of HSP in patients with stroke have been provided.

Incidence and Temporal Presentation

Longitudinal studies have suggested that nearly 75% of patients with hemiplegia experience HSP during the 12 months after stroke (Price & Pandyan, 2001). It is recognized that HSP not only occurs in the early stage but also persists in the chronic stage of stroke. In a large population-based prospective study of 1,761 patients with stroke, shoulder pain was reported by 17% of participants at 1 week, 20% of patients at 1 month, and 23% of participants at 6-month follow-up (Ratnasabapathy et al., 2003). Although HSP can present as early as 1 week poststroke, it most commonly occurs 8-10 weeks poststroke (Koog et al., 2010). A New Zealand study of 76 acutely admitted patients in the initial 12 weeks after stroke illustrated the temporal onset of HSP in more detail. The highest incidence (24% at rest and 58% on movement) was found at 10 weeks poststroke, whereas the lowest incidence occurred in the first week after stroke (12% at rest and 35% on movement; Bender, & Mckenna, 2001). According to the abovementioned studies, the commencement of HSP is not uniform, and the time frame within which it may occur is extensive. The temporal development of HSP and variability among stroke survivors may be driven by variable mechanisms.

Etiology and Outcomes

The mechanisms underlying the development of HSP are not well understood and are complex. They involve both nociceptive and neuropathic mechanisms in both the peripheral and central nervous systems (Roosink, Renzenbrink, Geurts, & Ijzerman, 2012a; Vuagnat & Chantraine, 2003). The occurrence of HSP has historically been attributed to biomechanical alterations within the shoulder joint. Many unidimensional interventions were developed focusing on regional treatment around the affected shoulder joint; however, none was found to be beneficial to all patients, and many continued to have significant pain. HSP that persists beyond 3 months is termed "persistent poststroke shoulder pain." It occurs in approximately 65% of patients with poststroke shoulder pain (PSSP; Lindgren et al., 2007). Studies exploring the treatment of PSSP have not been fruitful, and most sufferers do not experience relief. The relatively high incidence of persistent PSSP and the ineffectiveness of PSSP treatment suggest that it may not be merely because of simple nociception from the shoulder joint (Roosink, Renzenbrink, Geurts, & Ijzerman, 2012b). There is evidence that HSP is linked to central poststroke pain (CPSP). CPSP is defined as pain and sensory abnormalities in the body parts that correspond to the brain territory that has been injured by the cerebrovascular lesion (Klit, Finnerup, & Jensen, 2009). The clinical presentations of PSSP and CPSP show considerable overlap, and in some cases, it may be difficult to differentiate the two (Roosink, Buitenweg, Renzenbrink, Geurts, & Ijzerman, 2011; Smith, 2012). HSP has also been associated with altered somatosensory function and reduced cognitive-evaluative cortical somatosensory processing (Roosink et al., 2011, 2012). This conclusion was derived from an explorative study, which compared chronic PSSP patients (n = 6) with patients with pain-free stroke (n = 14) and healthy controls (n = 20). Cortical potentials were recorded after intracutaneous electrostimulaton using electroencephalogram, whereas sensory examination was performed using clinical examination and quantitative sensory testing. In all patients with stroke, reduced evoked potential amplitudes (N150, P300) and increased evoked potential latencies (N90, N150, P300) were found in response to stimulation at both the affected and unaffected sides. In addition, PSSP was associated with increased P200 and N150-P200 peak-to-peak latencies after stimulation at both sides. At the affected side, diminished cold sensation and proprioception were more often observed in patients with stroke (PSSP and pain-free stroke) as compared with controls.

HSP is a refractory poststroke complication caused by multiple factors. There is no clear consensus on the relative importance of these factors. In a review of English language articles between 1990 and 2000, an association between HSP and the clinical diagnoses of shoulder-hand syndrome, altered sensitivity, rotator cuff tear, subluxation, and adhesive capsulitis was established. This work also indicated loss of shoulder external rotation range because subscapularis muscle spasticity was a significant component of a painful hemiplegic shoulder (Bender & Mckenna, 2001). Another systematic review reported exactly the same causation of HSP (Turner-Stokes & Jackson, 2002). Subsequent work identified several neurophysiologic mechanisms, including weakness, muscle imbalance, spasticity, or abnonnal patterns of activation, as the underlying causes behind the clinical manifestations of shoulder pain (Fotiadis, Grouios, Ypsilanti, & Hatzinikolaou, 2005). Recently, a retrospective study including 94 patients (the days of onset to admission varied from 3 to 181, and the length of inpatient stay varied from 7 to 153) explored the association between four predictors (shoulder range, Motor Assessment Scale items, subluxation, and altered sensation) and shoulder pain and found that reduced active control and passive range of motion at the shoulder appeared to be risk factors for shoulder pain during inpatient rehabilitation poststroke. It is also noted that shoulder pain was present in one in four participants at admission to rehabilitation and one in three participants during inpatient period (Blennerhassett, Gyngell, & Crean, 2001). In addition, the upper extremity is especially prone to tissue damage because of its abundant degrees of (motion) freedom and its important role in many activities of daily living (Roosink et al., 2012b). Therefore, incorrect moving and handling may result in trauma and the onset of HSP (Fotiadis et al., 2005; Koog et al., 2010; Smith, 2012). Providing the patient under arm assistance to stand or walk, pulling on the affected arm, or any attempt to move the arm actively or passively without correcting the abnormal shoulder complex alignment during movement may actually initiate or exacerbate HSP symptoms. Shoulder pain is a distressing complication of stroke, which interferes with both function and QOL. Reduced participation in functional activities and the rehabilitation process have been reported for patients who develop HSP (Bender & Mckenna, 2001; Turner-Stokes & Jackson, 2002). Furthermore, a protected and immobilized shoulder interferes not only with upper limb function but also with balance, walking, transfers, and performance of self-care activities. HSP can therefore impede the process of rehabilitation and has been associated with poorer outcomes and increased length of stay in hospital (Turner-Stokes & Jackson, 2002).

Interventions

Because of the multifactorial etiology of HSP, quite a number of interventions were developed in the past few decades. However, there is still considerable confusion about their effectiveness as variable etiologies likely result in the same complication. One-hundred seventy-five different types of interventions were identified through interview followed by a survey in the United Kingdom (Pomeroy, Niven, Barrow, Faragher, & Tallis, 2001). Snels, Beckerman, Lankhorst, and Lex (2000) reported 54 different combinations of treatments, which were classified into eight treatment groups. The frequency of the first choice of treatment was physiotherapy (32%). Evidence-based interventions remain limited although many studies have been conducted in this area since the 21st century. The focus of the remainder of this article is on the current evidence for managing patient care for the purpose of improving HSP. Table 1 provides an overview of the interventions discussed and their reported efficacy in HSP.

Electrical Stimulation (Physiotherapy)

Electrical stimulation (ES) is frequently applied by two common methods in the clinical setting. Functional ES (FES), often called neuromuscular ES (NMES), stimulates the motor nerves innervating muscles, causing their contraction in an organized fashion to facilitate the recovery of limb function, reduce spasticity, or create better alignment of a joint's articular surfaces. Transcutaneous electrical nerve stimulation (TENS) stimulates the sensory nerves and is often used specifically as an analgesic technique to mask pain by giving lower-intensity, higher-frequency stimulation to cutaneous peripheral nerves without causing muscle contraction. The implications for these two techniques are not clear because the indications, methods, and treatment effects of them overlap to some degree (Price & Pandyan, 2001).

ES is not a new technique. Most recent studies focus on the effectiveness of FES while treating HSP. FES generally includes three forms using either surface (transcutaneous), percutaneous, or implanted electrodes, respectively (Popovic, Popovic, & Keller, 2002). Before percutaneous implantable NMES, there was no evidence for any treatment to provide relief for chronic HSP from glenohumeral subluxation (Stolzenberg, Siu, & Cruz, 2012). A prospective, open-label-design pilot study including 15 stroke survivors with chronic (>6 months) HSP was performed by Renzenbrink and Ijzenuan (2004). After 6 weeks of percutaneous NMES (P-NMES), a significant reduction in pain was found, and it was still present at 6-month follow-up. The authors reported that P-NMES potentially reduced HSP and suggested future randomized controlled trials to establish the clinical value. A meta-analysis was carried out by Ada and Foongchomcheay (2002) to examine the efficacy of surface ES for the prevention or reduction of shoulder subluxation after stroke. Seven eligible randomized or quasirandomized trials including 183 participants of surface ES for shoulder subluxation treatment were included. It was found that surface ES combined with conventional therapy prevented, on average, 6.5 mm of shoulder subluxation (weighted mean difference, 95% CI [4.4, 8.6]) but only reduced ongoing subluxation by 1.9 mm (weighted mean difference, 95% CI [-2.3, 6.1]) compared with conventional therapy alone. Therefore, evidence supports the use of ES early after stroke for the prevention of shoulder subluxation but not for reduction of such subluxation later after stroke. However, Church et al. (2006) conducted a randomized controlled trial of 176 patients within 10 days of stroke onset and cautiously concluded that a 4-week program of surface NMES to the shoulder after acute stroke does not improve functional outcome and may worsen ann function in severely impaired patients with stroke. Thus, routine use of surface NMES to the proximal affected upper limb after acute stroke cannot be recommended.

Chae et al. (2007b) completed a secondary analysis of a multisite randomized controlled trial of intramuscular ES for HSP for the purpose of identifying predictors of treatment success and assessing the impact of the strongest predictor on outcomes. Thirty-two subjects were divided according to the median value of stroke onset: early (<77 weeks) versus late (>77 weeks), ft is concluded from this study that time from stroke onset was most predictive of treatment success. Stroke survivors who are treated early after stroke onset may experience greater benefit from intramuscular ES for HSP. Yu et al. (2004) found evidence supporting the use of intramuscular NMES in reducing HSP via a multicenter, single-blinded, randomized clinical trial involving 61 chronic stroke survivors. They confirmed that intramuscular NMES reduced HSP among those with shoulder subluxation, and the effect was maintained for at least 6 months after treatment. The subsequent report of the same research team further confirmed that intramuscular NMES reduced HSP, and the effect was maintained for more than 12 months after treatment (Chae et al., 2005). NMES is more effective for early stroke survivors and has a more lasting effect on HSP than alternative methods of treatment. Indeed, for the patients experiencing chronic shoulder pain, NMES might be the only remaining treatment option, yet the expensive cost and invasive procedures are restraints of early implementation of NMES. Therefore, if it is possible to identify the subgroup of patients with acute HSP who are most at risk for developing chronic HSP, this would enable intervention with P-NMES in an acute stage, resulting in possible cost savings (Van Til et al., 2006).

Vuagnat and Chantraine (2003) confirmed the important role of FES among the different therapeutic possibilities in acting on or decreasing shoulder pain, reducing disability in particular shoulder subluxation, and finally, improving motor function in a review of therapies for HSP. A latest review including two randomized clinical trials (RCTs) examined FES and also confirmed the positive outcomes with use of this treatment (Viana, Pereira, Mehta, Miller, & Teasell, 2012). However, conflicting results were found in a pilot study, which involved 23 patients with acute and subacute stroke with severe-to-complete arm and/or hand paralysis who were randomly assigned to the intervention group (n = 12) or control group (n = 11; Mangold, Schuster, Keller, Zimmermann-Schlatter, & Ettlin, 2009). This study did not find clear evidence for superiority or inferiority of FES and concluded that the duration of intervention should be at least doubled to test for superiority of FES in these highly impaired patients and approximately 50 participants would have to be assigned to each therapeutic intervention to find significant differences. Similarly, in an RCT involving 50 patients with stroke with HSP, insufficient evidence was found to recommend it for reducing or preventing HSP, although applying FES treatment to the supraspinatus and posterior deltoid muscles in addition to conventional treatment when treating the subluxation in hemiplegic patients is more beneficial than conventional treatment by itself (Koyuncu, Nakipoglu-Yuzer, Dogan, & Ozgirgin, 2010). As there were no restrictions in inclusion criteria related to disease duration for the trial, it indicated that a larger sample size may be required to explore differences in such a population.

In an RCT that aimed to compare the effects of two physical modalities, TENS and ultrasonic therapy (UST), on the patients with HSP, Moniruzzaman, Salek, Shakoor, Mia, and Moyeenuzzaman (2010) concluded that both were effective in pain reduction, increasing muscle strength, recovery of tenderness, and improvement of motor function, but TENS may be safer and superior to UST. It is important to note that studies of use of ultrasound UST in HSP are in its infancy, with few studies reported.

Acupuncture (Alternative and Complementary Technique)

Acupuncture is based on a complex traditional Chinese medicine (TCM) theory that is not easily comprehended. TCM encompasses a philosophical concept that the entire human body is composed of sophisticated interconnected inner systems. These systems should be in balance to maintain a good health. In TCM theory, there is an "energy (Qi or Chi)" that flows through "channels (meridian)" in each organ. Most acupoints are located along one of these channels, although there are exceptions. Diseases are caused by an imbalance or disturbance of Qi. Needling at the acupoints can harmonize Qi and cure diseases (Lin & Chen, 2009). Although the internal mechanism is not very clear, acupuncture therapy is widely implemented for treating pain and provides some relief for many patients.

In a recent systematic review of acupuncture for HSP conducted by Lee et al. (2012), RCTs involving the effects of acupuncture for HSP, published between January 1990 and August 2009, were obtained from the National Libraries of Medicine, MEDLINE, CINAHL, AMED, Embase, Cochrane Controlled Trials Register 2009, Korean Medical Database (Korea Institute of Science Technology Information, DBPIA, KoreaMed, and Research Information Service System), and the Chinese Database (China Academic Journal). Seven of the 453 studies that met the inclusion criteria for this review were included. All of the included studies were from China and reported positive effects of the treatment. The quality of the studies was appraised strictly by the Modified Jadad Scores and the Cochrane Back Review Group Criteria List for Methodologic Quality Assessment of RCTs. It was concluded from this systematic review that acupuncture combined with exercise was effective for HSP.

Most studies on acupuncture as a treatment of HSP are published in Chinese. This has limited their use in non-Chinese-speaking countries. There are different types of acupuncture that may have different effectiveness in treating HSP. In an RCT of 60 patients with stroke with HSP (Bai, 2010), either balance acupuncture or conventional acupuncture had significant analgesic effects on HSP. The instant analgesia effect of balance acupuncture was found to be superior to that of conventional acupuncture. This work has particular relevance as most studies performed in non-Chinese-speaking countries are likely to utilize conventional acupuncture. Another RCT confirmed the positive impacts of acupuncture (Zhang & Tang, 2011). Thirty patients with stroke with movement disorder were randomly assigned to one of three groups: a scalp acupuncture-training group, a body acupuncture group, and a medication group. After 8 weeks of intervention, shoulder pain and motor function were remarkably improved in all groups. Scalp acupuncture combined with physical therapy was identified as the most effective solution for HSP. More recently, Li et al. (2012) evaluated the clinical therapeutic effect of acupuncture combined with Tuina on HSP. Tuina is a form of Chinese manipulative therapy that uses specific manipulations or massage tools to operate on certain areas or acupoints on the surface of the body (Li, 2011). During a two-center randomized controlled clinical trial, 300 patients with stroke with HSP were randomized to receive electroacupuncture and Tuina (treatment group) or electrostimulation and proprioceptive neuromuscular facilitation (control group). After 6 weeks of treatment and 12 weeks of follow-up, shoulder pain and motor function of the upper limb were more obviously improved in the treatment group compared with the control group although the clinical incidences of shoulder-hand syndrome and shoulder joint subluxation of hemiplegia were equal. Therefore, this study identified that the combined therapeutic effect of electroacupuncture and Tuina was satisfying for patients with HSP.

Strapping and Sling (Supportive Device)

Strapping of the hemiplegic shoulder has been used as a supplemental technique for subluxation and shoulder pain. The aim of strapping is to facilitate or inhibit the musculature surrounding the scapula and promote normal alignment of the scapula in relation to the thorax, humerus, and clavicle (Bender & Mckenna, 2001). There is scant evidence to confirm the benefit of strapping in the treatment of HSP. A prospective, randomized, single-blind controlled trial of 98 patients within 3 weeks of stroke compared the effectiveness of strapping with no strapping in the management of HSP. Both groups received rehabilitation in an interdisciplinary team setting. No significant benefit with shoulder strapping was shown at the end of the 6-week treatment nor 2 months later. The authors identified eight possible rationale for the lack of significance in this study including incorrect technology, insensitive measurements, short period of intervention, negative effects of the slings, and severe disability (Hanger et al., 2000). Griffin and Bernhardt (2006) conducted another RCT involving 33 patients who presented to rehabilitation within 3 weeks of their stroke. After 4 weeks of intervention, pain was less likely to develop in those patients with therapeutic strapping compared with those without strapping or with placebo strapping. It is concluded from this study that therapeutic strapping the hemiplegic shoulder prevented development of shoulder pain. There are two additional reviews suggesting that the onset of the shoulder pain could be delayed by this technique (Ada, Foongchomcheay, & Canning, 2005; Smith, 2012). The most recent RCT performed by Pandian et al. (2013) is the largest study to date. This study randomized 162 first-ever patients with stroke within 48 hours of stroke onset to receive shoulder taping versus sham taping for 2 weeks. Although not statistically significant, there was a trend toward pain reduction and functional improvement associated with shoulder taping. In addition, strapping is less expensive than other interventions and was therefore recommended by the author to be widely implemented in patients with stroke during acute stage.

There is rare evidence concerning the benefit of sling in the use of controlling shoulder pain after stroke. In a recent review, it was determined that there was insufficient evidence to confirm slings as an effective approach for preventing subluxation, reducing HSP, or increasing function after stroke (Smith, 2012).

Handling, Positioning, and Massage (Nursing Practice)

In considering that stroke care provided by neuroscience nurses includes transferring, positioning, and assisting in activities of daily living, it is clear that nurses are an important part of the therapy process (Seneviratne, Then, & Reimer, 2005). Appropriate nursing techniques could avoid shoulder injury in patients with stroke. Although related evidence is limited, a latest review recommended a number of nursing practices regarding assistance and positioning techniques based on a series of clinical guidance. For example, the arm should be moved slowly and be rotated outward when lifted to avoid impingement; the position of the shoulder should be checked when the patient is assisted to move in bed; and it should be ensured that the scapula glides forward, particularly when lying on the hemiplegic side (Smith, 2012). Furthermore, Mok and Woo (2004) recommended slow-stroke back massage as an effective nursing intervention for reducing the patients' levels of shoulder pain perception and anxiety in elderly patients with stroke via an experimental quantitative study involving 102 participants.

Tyson and Chissim (2002) reported a therapeutic technique of range of movement in the hemiplegic shoulder with help in an RCT including 22 participants. The study randomized patients to "usual care" versus a specific technique of lifting the hemiplegic arm by holding the humems under the axilla and maintaining external rotation (see Figure 1, available as Supplemental Digital Content 1 at http://links.lww.com/JNN/A15). They found that the specific technique resulted in greater range of motion at the hemiplegic shoulder than a "distal hold." Whereas, incorrect handling of patients, which is more likely to occur during usual care, may result in improper dynamic motor control and rotator cuff tearing. Thus, it is very important to remind caregivers to depress the humeral head when flexing the shoulder joint and to avoid overstretching the shoulder (Fotiadis et al., 2005).

The scapula is normally held on the thorax at an angle of 30[degrees] from the frontal plane. When the position of the scapula on the thorax is changed because of disturbed biomechanical factors contributing to glenohumeral stability, shoulder subluxation occurs (Fotiadis et al., 2005). Despite lack of empirical evidence, there were several recommended positions for the upper limb, such as abduction, external rotation and flexion of the shoulder, and moving and positioning the patient into a reflex inhibiting pattern (Bender & Mckenna, 2001).

Pharmacologic Therapies

Four RCTs on the topic of botulinum toxin A (BoNT/A) as a treatment of HSP were rigorously appraised in a systematical review by Koog et al. (2010). All studies without language restrictions were collected from searches of MEDLINE, CINAHL, EMBASE, and the Cochrane Controlled Trials Register from their inception to June 2008. When the effects of BoNT/A injection were assessed at 1 month or 3 months, it was found that this treatment was not useful for managing HSP, whereas intramuscular NMES is helpful up to 3 months. This review also reported that, although exact mechanisms have not been established in humans, BoNT/A was considered to have an antinociceptive effect that was separate from its neuromuscular blockade activity.

Some later reviews reported inconsistent results concerning the effectiveness of BoNT/A in treating HSP. In a systematic review performed by Singh and Fitzgerald (2011), five RCTs in patients with HSP found that an intramuscular injection of BoNT/A significantly reduced pain at 3-6 months and improved shoulder external rotation at 1 month. The work of Teasell, Foley, Pereira, Sequeira, and Miller (2012) concluded that botulinum toxin injected into the subscapularis muscle could reduce spastic shoulder pain and improve passive range of motion of the hemiplegic shoulder. A review aimed at identifying the effectiveness of therapeutic interventions targeting HSP more than 6 months after stroke was conducted by Viana et al. (2012). Articles published in the English language from 1980 to April 2012 were obtained. Among 10 RCTs, which met the inclusion criteria, three of them were with regards to the use of BoNT/A. Conflicting results were seen in the injection of BoNT/A.

Chae et al. (2007c) assessed the effectiveness of subacromial corticosteroid injections for the treatment of HSP through a retrospective chart review. This review involved 60 patients with HSP who were treated with a subacromial corticosteroid injection to the affected joint between January 1, 2005, and June 30, 2007. The authors prudently concluded that subacromial corticosteroid injection was associated with a significant reduction in HSP. It is important to note that there were no RCTs in this area, and these are needed to show a cause-and-effect relationship and mle out spontaneous recovery, placebo effect, and other confounding factors. Then, an exploratory, prospective case series study including 10 stroke survivors experiencing HSP with the treatment of subacromial corticosteroid injection during a 12-week period came to a similar conclusion; however, a gradual loss of effect with time was identified in this study (Chae & Jedlicka, 2009). A latest review involved three RCTs focusing on intra-articular glenohumeral corticosteroid injections and one RCT addressing the use of subacromial corticosteroid injections. The efficiency of the use of corticosteroid injections in HSP was noted by the reviewers (Viana et al., 2012).

In an RCT conducted by Lakse, Gunduz, Erhan, and Celik (2009), 38 patients with stroke with shoulder pain caused by frozen shoulder and impingement syndrome were assigned randomly into either injection (either intra-articular or subacromial injections of corticosteroid and local anesthetic according to their pathology) or control groups. TENS and the therapeutic exercise program were applied to both groups. Significant improvements in HSP and range of motion were found in both groups. Pain reduction in the injection group was more significant than the control group at the end of the first and fourth weeks. In addition, increases in shoulder range of motion were more significant in the injection group. Therefore, corticosteroid combined with prilocaine injection can be a good treatment option for appropriate HSP patients. Fifty-eight HSP patients with evidence of rotator cuff disorder were enrolled in a multicenter, randomized, triple-blind, placebo-controlled trial. They were randomly assigned to receive ultrasound-guided subacromial injection with triamcinolone (treatment group, n = 29) or lidocaine (placebo group, n = 29). After 8-week follow-up from the single injection, subjects receiving subacromial corticosteroid injection showed improved pain, disability, and active range of motion, and the duration of its efficacy continued up to 8 weeks (Rah et al., 2012). Yasar et al. (2011) performed an RCT including 26 patients more than 8 months after stroke. Intra-articular steroid injection was performed in 11 (42%) patients, and suprascapular nerve block (SSNB) was performed in 15 (57%) patients. In 4-week follow-up, both injection procedures were safe and had a similar effect in patients with stroke with HSP.

Two RCTs have evaluated the use of SSNB in HSP. In a small sample, Boonsong, Jaroenarpornwatana, and Boonhong (2009) showed that SSNB was a safe and effective treatment for HSP. It was more rapid and effective than therapeutic ultrasound in reducing pain but showed similar improvement in range of motion after 4 weeks. Allen, Shanahan, and Crotty (2010) conducted a double-blind RCT of 66 patients with HSP to identify the effects of SSNB as part of an interdisciplinary approach to the treatment of shoulder pain after stroke. Both groups continued to receive routine standard care including physiotherapy. This study found pain symptom reduction in mechanical shoulder pain and improved upper limb function.

Discussion

Evidence supporting specific intervention(s) for the management of HSP is limited. Recent conclusions from the studies focusing on this subject are revealed in this article to provide optional management for the clinical practice. ES, considered efficacious for several decades with minimal evidence, is still an approach of interest to be further explored in current studies. Another research focus is regional injection of medication in the hemiplegic shoulder. There is no clear consensus in favor of the implementation of these techniques because the studies of efficacy of all techniques were potentially biased by weak methodology, insufficient sample size, suitability of the intervention in specific stages of stroke, sensitivity of outcome measurements, duration of the intervention, and time length of follow-up. Thus, it implicates that the interpretation of these results should be cautious, and their implementation into practice requires consideration of clinical context. It is worth noting that acupuncture seems to be an effective treatment when dealing with shoulder pain in patients with stroke although the mechanism is unclear and not well accepted by western medicine. Nevertheless, a large number of the studies pertaining to this Chinese traditional technique utilized in HSP were written in Chinese, which has impeded the appraisal and promotion of acupuncture as a way in controlling HSP. In addition, nursing techniques involved in the article are not well supported except in recent studies. There are too few studies focusing on the role and specific maneuvers implemented by the nurse while caring for these patients. As an important part of the rehabilitation team, the role of the nurse in the reduction and prevention of shoulder pain poststroke should be further explored. Studies are needed to promote the practice and improve psychosocial adaptation in the patients with stroke experiencing shoulder pain.

The multifactor etiology of poststroke HSP and the distinction from CPSP require careful assessment before intervening. The evaluation should be conducted involving not only shoulder joint and surrounding soft tissue but also signs of a central lesion. Detailed assessment includes pain intensity; motor (active and passive) function of the upper limb; and somatosensory, cognitive, emotional, and autonomic functions as well as nonhemiplegic side, which is most likely to reveal the involvement of central pain mechanisms (Roosink et al., 2012b). Another issue worth consideration is the choice of proper measurement tools and methodologies used in research on HSP. Although clinical research must be carried out in the context of care provided, standardized assessment, measurement, and interpretation of findings are still achievable targets. Some functional deficits after stroke such as cognition, aphasia, and visuospatial neglects could impede the patient's ability to complete questionnaires accurately. Specific measurement tools appropriate to these patients need to be developed. Furthermore, measurement tools necessitate high level of reliability and validity to ensure precise interpretation of the efficacy of interventions. The third issue is the importance of regular assessment in terms of response to changes under interventions although they do increase workload.

HSP is a common and refractory complication after stroke. Multiple mechanisms likely underlie this complication and account for the variable efficacy of interventions in management of the subpopulation of stroke. Unidimensional interventions primarily aimed at the shoulder joint are often unsatisfactory especially in patients with persistent pain. Interventions should be multidimensional focusing on nociception as well as neuropathic lesions. The clinical manifestations of HSP could emerge early and may persist into the chronic phase after stroke. The results of this article indicate that appropriate preventive measures and timely response are needed to improve the individual patient outcomes. In view of the specific mixture of causes in an individual patient, tailored intervention programs based on the targeted evaluation could be helpful in the management of the syndrome. To improve the efficiency of management in HSP, it is reasonable to identify a number of critical areas that have a particular impact on outcome and develop an evidence-based multidisciplinary integrated care pathway (Jackson et al., 2002). Such a management model could also be used as a means of continuous quality promotion in clinical practice.

Conclusion

We report here on the current studies exploring the effectiveness of some interventions of interest in the management of HSP. ES, acupuncture, medication injection, and support device as well as best nursing practice reviewed in this article indicate variable efficacy. It is likely that each of these therapeutics, as well as acupuncture, provide some relief to HSP sufferers although no single treatment is efficacious in all patients. Careful assessment of the pain type and source of the pain can guide clinicians in selecting the ideal therapeutic to maximize pain relief for individual patients.

References

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Zheng Li, MSN, is a Senior Lecturer, School of Nursing, Fudan University, Shanghai, China.

Questions or comments about this article may be directed to Sheila A. Alexander, PhD RN, atsalexand@pitt.edu. She is an Associate Professor, Acute & Tertiary Care, School of Nursing, and Critical Care Medicine, School of Medicine, University of Pittsburgh, Pittsburgh, PA.

The authors declare no conflicts of interest.

Supplemental digital content is available for this article. Direct URL citations appear in the printed text and are provided in the HTML and PDF versions of this article on the journal's Web site (www.jnnonline.com).

DOI: 10.1097/JNN.0000000000000109
TABLE 1. The Definitions and Effectiveness of Included Interventions

Interventions     Definitions                Effectiveness

Electrical        Using electrical           The NMES is effective
stimulation       currents to cause          for early stroke
                  contraction of muscles     survivors and has a
                  or relieve pain (Price &   lasting effect on HSP
                  Pandyan, 2001)             with limited evidence,
                                             although there is rare
                                             evidence concerning the
                                             effectiveness of TENS in
                                             the use of controlling
                                             HSP.

Acupuncture       Using sharp, thin          Although the mechanism
                  needles that are           is unclear, acupuncture
                  inserted in the body at    seems like an effective
                  very specific points       treatment when dealing
                  (acupoints) to treat       with shoulder pain in
                  health conditions (The     patients with stroke .
                  Free Dictionary, 2013a)    Nevertheless, a large
                                             number of the studies
                                             pertaining to this
                                             Chinese traditional
                                             technique utilized in
                                             HSP were written in
                                             Chinese, which has
                                             impeded the appraisal
                                             and promotion of
                                             acupuncture as a way in
                                             controlling HSP

Strapping         Taping to a muscle to      Strapping is recommended
                  inhibit or activate        to be implemented in
                  activity (Bender &         patients with stroke
                  Mckenna, 2001)             during acute stage to
                                             prevent development of
                                             shoulder pain with scant
                                             evidence.

Sling             Using shoulder             The benefit of sling in
                  supportive device to       the use of improving HSP
                  hoist the limb (Smith,     is uncertain.
                  2012)

Handling,         Supporting the limb with   Lack of empirical
positioning,      someone's hands and        evidence regarding these
and massage       setting position (Smith,   specific techniques
                  2012); the rubbing or      implemented by nurses.
                  kneading of parts of the
                  body especially to aid
                  circulation, relax the
                  muscles, or provide
                  sensual stimulation (The
                  Free Dictionary, 2013b)

Pharmacologic     Referring to therapy       There is no clear
therapy           that relies on botulinum   consensus in favor of
                  toxin A, corticosteroid,   the implementation of
                  and nerve blockers (Chae   these techniques because
                  & Jedlicka, 2009; Yasar    the studies of efficacy
                  et al., 2011)              of all techniques were
                                             potentially biased by
                                             methodological reasons.
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Author:Li, Zheng; Alexander, Sheila A.
Publication:Journal of Neuroscience Nursing
Article Type:Report
Geographic Code:6MORO
Date:Feb 1, 2015
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