The effects of hemiplegic shoulder pain on upper extremity motor function and proprioception

Abstract

BACKGROUND:

Hemiplegic shoulder pain (HSP) after stroke has negative effects on functional use of hemiplegic arm.

OBJECTIVE:

This study aimed to investigate the effects of HSP on upper extremity motor function and proprioception.

METHODS:

Hundred and twenty-two patients with hemiplegia were included in this study. The patients’ shoulder pain was evaluated by Visual Analog Scale. According to pain scores, patients were divided into two groups as group with HSP (Group 1, n = 76) and group without HSP (Group 2, n = 46). Upper extremity motor function level and proprioception were assessed by using Fugl Meyer Motor Function Scale and the Laser-pointer Assisted Angle Reproduction Test for the 45°, 60° and 90° of shoulder flexion.

RESULTS:

Upper extremity motor function and shoulder’s proprioceptive sense at each angles of group 1 were found significantly worse than group 2’s (p≤0.005). Correlation analysis revealed a significant positive correlation between HSP severity, and upper extremity motor dysfunction and proprioceptive impairment (p < 0.005).

CONCLUSIONS:

Presence of HSP is one of the main determinators of upper extremity motor function level and proprioceptive ability at different angles. Management of HSP can make a significant contribution to sensorimotor integration by leading to recovery in the motor function and proprioceptive acuity.

Keywords

Stroke hemiplegia shoulder pain upper extremity Visual Analog Scale proprioception

1 Introduction

Hemiplegic shoulder pain (HSP), reported frequency as 65–70%, is one of the most common symptoms in stroke survivors. HSP has a multifactorial etiology including social, emotional and biomechanical factors (Adey-Wakeling et al., 2015). Persistent shoulder pain leads to reduce functional use of the hemiplegic arm. Many stroke patients with HSP limit their shoulder movements in different directions. The non-functional shoulder not only affects upper extremity performance, but it also causes activity avoidance and less balance control during walking and transfer activities. Thus, HSP complicates the daily living activities (Turner-Stokes et al. 2002).

In patients with stroke, it has been demonstrated that pain is associated with motor and sensory disturbance, spasticity, musculoskeletal system problems, etc. (Chae et al. 2007). Because the pathological mechanism of HSP is not clearly defined, a satisfactory treatment with high efficacy has not been developed yet. However untreatable shoulder pain causes secondary problems which limit upper extremity function (Yi et al. 2013). Sensory deficits, shoulder trauma, inferior shoulder subluxation, spasticity, adhesive capsulitis, heterotopic ossification, etc., which can be defined as secondary problems to stroke, can also cause HSP. So, this leads to an infrangible circle (Chae et al. 2007, Manara et al. 2015).

Another common post-stroke sensory complication is proprioceptive impairment. Loss of proprioception, which leads to functional disability in patients with stroke, affects the ability of detecting extremity localization. Proprioceptive impairments complicate both the control of extremity motion and regaining motor function in patients with stroke (Carey et al. 1993, dos Santos et al. 2015). The proprioception is also deteriorated via the dysfunction of peripheral and central structures due to the changes in reflex activity and gamma motor system sensitivity in presence of pain. Because the patients with pain cannot make a comparison between the planned and performed movement, they lose feedback and feedforward ability (Niessen et al. 2008, Roijezon et al. 2015).

Further studies are needed to clarify secondary symptoms affected by shoulder pain. This study was designed to evaluate the effects of shoulder pain on upper extremity function and proprioception, and to identify their relationship in patients with stroke.

2 Materials and methods

2.1 Participants

This study was conducted in 76 patients with HSP [33 (43.3%) female, 43 (56.6%) male] and 46 patients without HSP [17 (37%) female, 29 (63%) male] attending the physical therapy and rehabilitation department. Volunteer participants who suffered stroke at least 1 month prior, scored more than 24 points on the Mini Mental State Examination, and had increased muscle tone in shoulder extensors (grade 1 or 2 according to Modified Ashworth Scale) were included in this study. Patients with shoulder pain due to another reason such as trauma, another neurological disease, blindness and deafness were excluded (Fig. 1). All procedures were in accordance with the Declaration of Helsinki. The study was approved by the Ethics and Human Research Committee of Pamukkale University Hospital (Denizli, Turkey). IRB approval was obtained with number 60116787-020/59257. Each patient gave written informed consent.

Fig. 1

Flowchart of patient inclusion.

2.2 Procedure

After demographic characteristics including age, body mass index (BMI) and medical status of participants (hemiplegic side, disease duration, and cause of stroke) were recorded, the shoulder pain severity was assessed by Visual Analog Scale (VAS) during rest and active shoulder flexion. Participants were divided into two groups as the group with HSP (group 1) and the group without HSP (group 2) according to presence of HSP determined by using VAS. Upper extremity motor impairment was assessed by the Fugl Meyer Motor Assessment Scale (FMMAS) for a total of 122 volunteers included in the study. The Laser-pointer Assisted Angle Reproduction Test was used for evaluation of proprioception at 45°, 60° and 90° of shoulder flexion. Proprioception test was repeated three times and the mean result of three measurements pointed the proprioceptive deviation.

FMMAS is a stroke-specific, performance-based impairment index. Upper extremity motor function sub-section was applied to determine disease severity and describe motor recovery. Items are scored on a 3-point ordinal scale as 0 = cannot perform; 1 = performs partially; 2 = performs fully. Maximum Score for upper extremity motor function is 66. The FMMAS is completed in maximum 30–45 minutes (Rand et al. 2012).

Two round plates divided into 360 pieces were fixed to the two stable surfaces looking at each other for The Laser-pointer Assisted Angle Reproduction Test. Two thermoplastics over sleeves, which had 3 laser pointers pointing round plates, were worn to both arms of the patient. Both tuberculum majus of the patient were considered as pivots and placed in the center of these two chambers. After the test was explained to the patient, sense of sight and hearing were blocked by using a couple of headsets and an eye patch. While the eyes of the patient were closed, the hemiplegic shoulder was flexed at 45° of shoulder flexion for three times by following the trace of the laser pointer and patient was instructed to memorize this position. Then the arm was returned to starting position. The same movement was repeated 3 times with contralateral shoulder. The trace of the laser pointer was marked on a round plate. The scores pointing how much the shoulder flexion of non-hemiplegic arm deviated from 45° for each of the 3 measurements were recorded. Average of 3 deviations was calculated and noted. The same procedure was repeated to test the position sense at 60° and 90° of shoulder flexion (Ager et al. 2019, Balke et al. 2011).

2.3 Statistical analysis

The statistical package SPSS 21.00 for Windows (SPSS Inc., Chicago, IL, USA) was used for statistical analysis. All continuous variables were evaluated for normality using Kolmogorov-Smirnov test. Continuous variables were expressed as mean±standard deviation (if data were normally distributed) or as medians in combination with quartiles and percentiles (if data were not normally distributed). FMMAS and angle deviations at the angles of 45° of shoulder flexion data of groups were compared with Mann–Whitney U test because of non-normal distribution. Since angle deviation at the angles of 60° and 90° of shoulder flexion data were distributed normally Independent Sample t test was used to compare the results. In group analysis, the correlation of VAS scores, FMMAS scores and angle deviations was determined by Spearman Correlation Analysis. Level of significance was set at p < 0.05.

3 Results

Average age was 61.54±16.33 years in group 1 and 55.93±16.58 years in group 2. When the affected side of the participants were analyzed, it was observed that there were 36 (47.4%) right and 40 (50.2%) left hemiplegia in group 1 and 24 (54.2%) right and 22 (47.8%) left hemiplegia in group 2. There were no statistically significant differences between the groups in terms of demographic data (p > 0.05) (Table 1).

Table 1
Baseline characteristics of the groups

Group 1 (Group with HSP) Group 2 (Group without HSP) p ^*

Age (years) 61.54±16.33 55.93±16.58 0.70^*

BMI (kg/m²) 26.94±4.70 26.89±4.55 0.96^*

Gender [n (%)] Female 43 (56,6%) 29 (63%) 0.48

Male 33 (43,3%) 17 (37%)

Hemiplegic side [n (%)] Right 36 (47.4) 24 (54.2) 0.60^**

Left 40 (52.6) 22 (47.8)

Medication^* [n (%)] 6 4,5 0.48^†

4–7 2.5 –7

		Group 1 (Group with HSP)	Group 2 (Group without HSP)	p ^*
Age	(years)	61.54±16.33	55.93±16.58	0.70^*
BMI	(kg/m²)	26.94±4.70	26.89±4.55	0.96^*
Gender [n (%)]	Female	43 (56,6%)	29 (63%)	0.48
	Male	33 (43,3%)	17 (37%)
Hemiplegic side [n (%)]	Right	36 (47.4)	24 (54.2)	0.60^**
	Left	40 (52.6)	22 (47.8)
Medication^* [n (%)]		6	4,5	0.48^†
		4–7	2.5 –7

BMI: Body Mass Index ^†: Mann-Whitney U test, expressed as medians in combination with quartiles and percentiles (% 25–% 75). ^*: Independent Sample t test. ^**: chi squared test.

The pain intensity of group 1 during rest and activity were 3.27±3.50 and 6.48±3.07, respectively. Figures 2 and 3 show the FMMAS scores and angle deviations at 45°, 60° and 90° of shoulder flexion of the groups. While the minimum angle deviations were acquired at 90° of shoulder flexion and maximum angle deviations were seen at 45° of shoulder flexion in both groups. Table 2 shows the comparison of FMMAS scores and proprioception test scores (absolute errors) for 45°, 60° and 90° of shoulder flexion of the patients with and without HSP. The group with HSP showed significantly worse FMMAS scores than those patients without HSP (p = 0.005). When comparing the angle deviation scores, the deterioration of proprioception sense in group 1 was worse than group 2 in all reference angles (p < 0.05). The maximum difference in terms of deviations was observed for the measurement of shoulder proprioception at 45° of shoulder flexion between the groups (p = 0.000) (Table 2). Analysis of relationship between the VAS, FMMAS and proprioceptive acuity of group with HSP demonstrated that VAS scores had a negative significant correlation with FMMAS scores and positive significant correlation proprioceptive deviation (p < 0.05) (Table 3).

Fig. 2

FMMAS scores of the groups.

Fig. 3

Angle deviations at 45°, 60° and 90° of shoulder flexion of the groups.

Table 2

Comparison of FMMAS scores and absolute errors at 45°, 60° and 90° of shoulder flexion of patients with and without HSP

		Group 1 (n:76)	Group 2 (n:46)	p
FMMAS	Total score	40 (9.75 –60)	57.5 (32.25 –64)	0.005^†
Absolute errors at 45° of shoulder flexion	Mean score	7.67 (4.41 –11)	2.83 (1.91 –4.08)	0.000^†
Absolute errors at 60° of shoulder flexion	Mean score	4.91±2.61	3.32±2.33	0.001^*
Absolute errors at 90° of shoulder flexion	Mean score	4.61±3.45	3.00±3.04	0.010^*

FMMAS: Fugl Meyer Motor Assessment. ^†: Mann-Whitney U test, expressed as medians in combination with quartiles and percentiles (% 25–% 75). ^*: Independent Sample t test. boldface p values were statistically significant.

Table 3

Correlation between HSP and FMMAS scores and absolute errors at 45°, 60° and 90° of shoulder flexion

		FMMAS	AE at 45°	AE at 60°	AE at 90°
VAS_rest	r	–0.337^**	0.278^*	0.519^**	0.230^*
	p	0.003	0.015	0.000	0.045
VAS_act	r	–0.435^**	0.449^**	0.582^**	0.534^**
	p	0.000	0.000	0.000	0.000

VAS_rest: Visuel Analog Scale during rest; VAS_act : Visuel Analog Scale during activity; FMMAS: Fugl Meyer Motor Assessment; AE at 45°: absolute errors at 45° of shoulder flexion; AE at 60°: absolute errors at 60° of shoulder flexion; AE at 90°: absolute errors at 90° of shoulder flexion. Pearson rank test, ^*: p < 0.05; ^**: p < 0.01.

4 Discussion

The goal of this study was to identify the relationship between the shoulder pain, upper extremity motor function level and proprioception sense in patients with stroke. It was found that (1) patients with HSP show less upper extremity motor function than patients without HSP; (2) shoulder proprioception sense gets worse with presence of HSP compared to the shoulder without pain; (3) the proprioception deficits are greater in low-angle shoulder flexion positions; (4) while severity of HSP increased, both upper extremity motor and proprioceptive impairment increased.

Secondary changes in biomechanical alignment of the upper limbs resulting from HSP can cause avoidance from certain movements or activities such as lifting the arm, eating or leisure time activities (Lindgren et al. 2019, Yi et al, 2013). This mechanism mentioned in the literature explains how HSP makes patient’s life difficult and increases the level of dependence by damaging sensory-perceptual-motor integration. Since persistent shoulder pain causes decreased and abnormal upper extremity function, recovery is delayed (Teasell et al. 2009). We found in the present study that shoulder pain significantly lowered the upper extremity motor function level in patients with stroke. This finding is consistent with reports of the studies pointed to togetherness of HSP and low Barthel Index scores indicating the upper extremity malfunction. This interesting finding suggests the necessity of preventive interventions to be implemented by neurorehabilitation professionals before onset of HSP (Lindgren et al. 2007, Paci et al. 2007). Because poor motor function was also defined as one of major risk factors for HSP (Karaahmet et al. 2014), repeated passive motion exercise without pain was also known to be helpful in improving sensory-perceptual-motor integration in patients with hemiplegia (Baek et al. 2009). If the treatment can be started as soon as the HSP occurs, we are of the opinion that an accelerated improvement in the motor function can be achieved (Lindgren et al. 2019).

Although the effects of HSP on the motor components of sensorimotor integration have been discussed in the literature extensively, it is still unknown how HSP changes proprioceptive signals during central processing. It is only hypothesized called as final common input that nociceptive signals interfere with proprioceptive signals and disrupt the motion decision (Ager et al. 2019, Weerakkody et al. 2008). The affiliation between pain and proprioceptive ability must be recognized because it has clinical importance to optimize proprioceptive clinical tools and to decide the rehabilitation programme (Ager et al. 2019). However, it is seen that the number of researchers interested in proprioception in patients with stroke is very low. Most researchers, who are interested in the relationship between shoulder pain and thumb proprioception (not shoulder proprioception), use only correlation and regression analysis to investigate togetherness of pain and proprioception. Similar to our results, in the light of these studies, it is possible to reach a general conclusion that proprioceptive sensitivity decreases as the pain increases (Blennerhassett et al. 2010, Lindgren & Brogardh 2014, Roosink et al. 2011), but it is difficult to say at which joint position proprioceptive sense impairment is the greatest in patients with hemiplegia.

In addition to general correlations and regression analyzes, there are a small number of studies examining whether shoulder pain is associated with positional sensation at different shoulder angles. Niessen et al. found that shoulder pain impaired the proprioception sense at four different reference angles of shoulder internal and external rotation in patients with stroke (Niessen et al. 2009). Although the results could imply more proprioceptive loss at lower rotational degrees, it is very difficult to make a clear judgment that the proprioception decreases as the angle increases. In addition to Niessen et al., there are studies examining the relationship between shoulder problems and angular positional difference in healthy individuals. The results of these studies will undoubtedly contribute to the interpretation of our findings because of quantitative data inadequacy. A study discovered that repositioning errors differ significantly at different angles of shoulder joint and at different body positions (supine, supine, upright posture) in healthy subjects. High positioning errors were seen at 90° and 110° of shoulder elevation, while there was no significant deviation at 70° of shoulder elevation (Suprak et al. 2016). Balke et al. compared proprioception acuity at 55°, 90° and 125° of shoulder flexion in the healthy and destabilized shoulders using the Laser-pointer Assisted Angle Reproduction Test. They found that while cases with healthy shoulder showed the best position sense (minimum error) at 90° of shoulder flexion and the worst position sense (maximum error) at below 55° of shoulder flexion, shoulder flexion performance was better at the angle of 125° than the angles of 55° and 90° in unstable shoulder (Balke et al. 2011). The results of Balke are in accordance with our findings that showed participants of both groups have better position sense at the wider angles and there is a significant difference between the two groups at the acute angles. Our results, relatively supported by the studies (Balke et al. 2011, Niessen et al. 2009), suggested that positional awareness at angles of 90° and positional errors at lower angular values are higher in a painful shoulder. It is necessary to consider this effect to increase the quality of movement during planning of neurorehabilitation and sensorimotor integration therapy (Findlatter & Dukelow 2017). According to our findings, we can say that recovery of gross motor movements is easier, but the improvement of activity-specific stabilization skills, requiring acute angles, is more difficult (Namdari et al. 2012). Because pain negatively affects the function of proprioceptors, including joint receptors and muscle spindles, narrow-angled fine motor skills that require more proprioceptor activity may be affected more. So, clinicians should not focus only on the motor component of movement in rehabilitation programs, but the treatment should be formed by evaluating the presence of HSP and the degree of proprioceptive impairment (Findlatter & Dukelow 2017). Management of HSP can make a significant contribution to sensorimotor integration by leading to recovery of motor function and proprioceptive acuity.

The difficulty of proprioception measurement, inadequacy of information, and the unwillingness of researchers to study about proprioception have led to the failure to enlighten the relationship between HSP and proprioception until now. Studies related to shoulder proprioception have been usually performed in patients with orthopedic problems. Our study is a premise study that evaluates shoulder proprioception comprehensively in patients with stroke. At the same time, we have strengthened our results with higher participation rates and objective methods than the other studies in the literature. In addition, although age is one of the important factors affecting the proprioceptive sensation (Riberio & Oliveira 2007), similarity between our groups in terms of age and affected side increases our belief in the validity of our results.

There are several limitations to be discussed. First, a longitudinal study might be more objective, but our study was planned as a cross-sectional study. Secondly, the use of computer systems for the evaluations of proprioception could provide more objective results. Despite the limitations, we hope that these results will be addressed in ongoing studies. More randomized controlled studies are needed in patients with HSP in which motor function is evaluated at different angles.

In conclusion, the current study points to the simultaneous effects of HSP on both upper extremity motor function and proprioception. While presence of HSP impairs the motor function, proprioceptive deficit during shoulder flexion increases in patients with stroke. So, presence of HSP is one of the main determinators of upper extremity motor function level and proprioceptive ability at different angles. However, further analysis revealed that increasing severity of HSP has a negative linear effect on motor function and proprioceptive decision-making. Management of HSP can contribute to sensorimotor integration in daily living activities by enhancing motor function and proprioceptive acuity.

Conflict of interest

No conflict of interest was declared by the authors.

Footnotes

Acknowledgments

The authors would like to thank all participants.

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