Effect of scapular proprioceptive neuromuscular facilitation on shoulder pain, range of motion, and upper extremity function in hemiplegic patients

A randomized controlled trial

Abstract

Background and Purpose: 

Poststroke shoulder pain is one of the most prevalent impairments (34%–86%) and it hinders the performance of daily activities and also interferes with stroke rehabilitation. The purpose of this study was to examine the effect of scapular proprioceptive neuromuscular facilitation (PNF) on shoulder pain, range of motion (ROM), and upper extremity (UE) function in hemiplegic patients.

Methods: 

Thirty hemiplegic patients were recruited and randomly allocated to Group A (n = 15) and Group B (n = 15). Experimental group received conventional treatment plus scapular PNF-hold relax technique while control group received only conventional treatment comprised passive shoulder ROM and stretching exercises and transcutaneous electrical nerve stimulation for 12 sessions (4 sessions/week). The outcome measures used were visual analog scale, shoulder ROM, lateral scapular slide test, and Fugl-Meyer motor assessment.

Results: 

Statistical analysis showed significant change in shoulder pain and UE function in both the groups with no significant differences between the groups; significant improvement in shoulder ROM in both the groups (except internal rotation in controls) and between-group comparison favored the intervention; scapular position improved significantly in experimental group for position A while all postintervention scapular positions in both the groups showed concordance with position of scapula on unaffected side.

Conclusion: 

Scapular PNF has positive impact on poststroke shoulder pain and ROM, helps in strengthening of proximal muscles of UE, thereby correcting scapular alignment and improving the UE function in stroke patients.

Introduction

Stroke is a clinical syndrome characterized by the sudden development of a persistent focal neurological deficit secondary to a vascular event.[¹] Following vascular occlusion, an ischemic cascade begins which includes energy and sodium-potassium pump failure, an increase in intracellular calcium, depolarization, generation of free radicals, blood brain barrier disruption, inflammation, and apoptosis[²] leading to various impairments.

One of the most important and frequent complications of stroke is shoulder pain, with varying prevalence of 34%–86%[³] and develops usually between 2 weeks to 2 months.[⁴⁵] The etiology of hemiplegic shoulder pain is multifactorial.[⁶] Many underlying pathologies have been found to be causing hemiplegic shoulder pain, namely, adhesive capsulitis (50%), glenohumeral subluxation (44%), rotator cuff tear (22%), shoulder-hand syndrome (16%),[⁵] and other disorders such as heterotopic ossification, thalamic syndrome, and brachial plexus injury.[⁷]

Existing clinical practice for management for shoulder impairments involves basic range of motion (ROM) exercises, heating modalities, stretching of the spastic muscles, facilitatory, and inhibitory techniques, which are neither specifically directed toward the impaired motor control nor functional in nature. Other treatment techniques employed for the problems of hemiplegic shoulder are oral analgesics, strapping, transcutaneous electrical nerve stimulation (TENS), ultrasound, approaches such as neurodevelopmental techniques, Brunnstrom's method, motor relearning technique, proprioceptive neuromuscular facilitation (PNF), Rood's approach; more aggressive measures such as regional anesthesia, desensitization, sympathectomy, intra-articular corticosteroids, intramuscular botulinum injections for intractable sympathetic disorders, and spasticity.[⁴⁷]

Following any type of pain, there occurs an imbalance in the surrounding muscles secondary to inhibition and lack of proper activation. Evidence suggests the importance of reducing pain level, developing awareness in deep stabilizing muscles and correct activation rather than the isolated muscle training when training the patients with cortical disorder for motor control. Authors also advocate for the use of mental imagery, tactile, verbal, visual, tapping, weight bearing, and movement-oriented cues for better results.[⁸]

PNF is an approach to therapeutic exercise that combines functionally based diagonal patterns of movement with techniques of neuromuscular facilitation to evoke motor responses and improve neuromuscular control and function.[⁹] The main objective of performing the exercises in PNF pattern is to enhance the functional movement through facilitation, inhibition, strengthening, and relaxation of muscle groups.[¹⁰] Hallmarks of this approach to therapeutic exercise are the use of diagonal patterns and the application of sensory cues – specifically proprioceptive, cutaneous, visual, and auditory stimuli – to elicit or augment motor response.[⁹]

The scapular patterns targeting the scapular muscles can be administered in two diagonals: anterior elevation – posterior depression and posterior elevation – anterior depression. The exercises can be performed with the patient lying on the treatment table, on mat, sitting, or standing.[¹⁰] Scapular PNF techniques incorporate functional or diagonal patterns for performing the exercises and can be used to stretch or strengthen the muscles selectively. These techniques also help the muscles to relearn the normal timing of recruitment and amount of activation so as to maintain the balance between different groups of muscles.

One of the techniques utilized in PNF is hold relax technique. Hold relax technique is effective, simple, and pain-free technique which has potential to induce relaxation, improve flexibility, and reduce pain. The authors hypothesized that there will be an effect of scapular PNF-hold relax technique on shoulder impairments in patients with hemiplegia.

However, there is a paucity of literature relating to the effect of scapular PNF-hold relax technique on shoulder pain and reduced ROM and upper extremity (UE) function in patients with hemiplegia. Hence, the need arises to study the presence of any influence of scapular hold relax technique in poststroke shoulder impairments.

Methods

Study design

This study used a randomized controlled design to study the effect of scapular PNF on shoulder pain, ROM, and UE function. Approval of the project was obtained from the Ethical Committee of KLE Institute of Physiotherapy. Institutionally approved written consent was obtained before the study participation. Participants after their enrollment were randomly allocated into either (1) experimental group, receiving scapular PNF-hold relax technique and conventional treatment or (2) control group, receiving only conventional treatment.

Participants

Participants of either sex with hemiplegia were recruited from secondary and tertiary health-care centers in Belagavi, Karnataka, India. Patients were included if they were suitable according to following criteria (1) age group: 40–80 years, (2) diagnosis of first-ever stroke, (3) having shoulder pain, (4) restricted shoulder ROM, and (5) cooperative and willing to participate. Patients were excluded if they had (1) any other diagnosed cause of shoulder pathology (fracture etc.,) not associated with stroke, (2) acute stroke (flaccid stage), (3) shoulder subluxation, (4) inability to follow the commands, and (5) other neurological disorders.

Outcome measures

Shoulder pain and ROM (viz., flexion, abduction, external and internal rotation) were assessed at baseline and after the completion of 12 session protocol using visual analog scale and goniometer, respectively. Other two outcome measures used in this study are as follow:

Lateral scapular slide test

Static scapular alignment was assessed using lateral scapular slide test (LSST) developed by Kibler which assesses the difference in side-to-side measurements of scapular distance in 3 test positions. Position A involves placement of the shoulder in glenohumeral joint neutral (arms at side). In position B, the humerus is placed in a position of medial rotation, with 45° of shoulder abduction in the coronal plane (hands kept on waist). In position C, the UE is placed in a position of maximal medial rotation, with 90° of shoulder abduction in the coronal plane. Measurements of scapular position are taken bilaterally from the inferior angle of the scapula to the spinous process of the thoracic vertebra in the same horizontal plane (the reference vertebra) in all 3 test positions. More recently, Kibler changed the threshold of bilateral difference (in scapular distance) of >1.0 cm to 1.5 cm to state the scapular symmetry as abnormal or deranged.[¹¹]

Fugl-Meyer assessment scale upper extremity

The Fugl-Meyer motor assessment scale includes items dealing with the shoulder, elbow, forearm, wrist, and hand in the UE and the hip, knee, and ankle in the lower extremity. It includes the assessment of reflex and voluntary activity, dominance of various synergies, sitting and standing balance, sensation in both the upper and lower extremities, and ROM of eight joints, four in each extremity. It is an impairment measuring scale which consists of 155 items. Each item in this scale is rated on a three-point ordinal scale (0: Not able to perform, 1: Able to perform partially, and 2: Able to perform completely).[¹²]

In the current study, only component A (UE) was taken to examine the effect of the intervention on UE function which gave the maximum score of 36. Component A included (1) reflex activity, (2) voluntary movement within synergy, (3) voluntary movement mixing synergy, (4) voluntary movement with little/no synergy, and (5) normal reflex activity. The three components of Fugl-Meyer assessment scale-UE, namely, wrist, hand, and coordination were not included as the intervention administered did not have any direct influence over these components.[¹³]

Procedure

The patients in experimental group received scapular PNF-hold relax plus conventional treatment. The session began with 30 min of conventional treatment including passive ROM exercises, passive stretching, and TENS (100 Hz - painful area method) followed by PNF-hold relax technique. Familiar to most clinicians, this technique involves lengthening a tight muscle and asking the patient to isometrically contract it for several seconds. As the patient relaxes, the clinician lengthens the involved muscle further and holds the stretch at the newfound end-ROM.[¹⁴] This study used the protocol consisting of 3 sets of 10 repeated scapular movements in the diagonal pattern of anterior elevation and posterior depression. The control patients received conventional treatment measures. Both the groups underwent the same protocol of 12 sessions (4 sessions/week). The outcome measures were assessed once again 12 sessions.

Data analysis

Statistical analysis of the data obtained was done using Statistical Package of the Social Sciences (SPSS, IBM, Bangalore) Version 20. Kolmogorov–Smirnov test was used to test the normality of pre- and post-intervention values. Paired and unpaired t-tests were used to assess within group and between-group differences, respectively. Unpaired t-test was used for comparing the two parameters obtained from LSST (unaffected side scapular distance versus affected side – postintervention distances). Probability values <0.05 were considered statistically significant and probability values <0.001 were considered highly significant.

Results

We screened 51 individuals with hemiplegia and enrolled 30 participants in our study; all the participants completed the study. No significant harms or unintended effects were found during the study. The flow of participants through the trial is summarized in Figure 1. All the demographic features were nonsignificant upon between-group comparison implying the homogeneous distribution. The baseline values recorded for each outcome measure were compared between groups which elicited nonsignificant results stating that the severity and status of the patients in both the groups was distributed homogeneously (P > 0.05). The demographic characteristics of each group are summarized in Table 1.

Figure 1: Consort diagram illustrating the flow of participants through the trial

Table 1: Demographic and baseline characteristics of patients (n=30)

Table 2 demonstrates the baseline and postintervention values of the outcome measures. The pain as per VAS score reduced significantly in both the groups but between-group comparison demonstrated no significance. Regarding shoulder ROM, there was significant improvement in all the ranges within both the groups (except internal rotation in control group), and upon between-group comparison, experimental group showed significantly larger gains in ROM (except external rotation).

Table 2: Within and between group comparison for the outcome measures

Scapular alignment did improve significantly in experimental group, but the improvement was limited to position A, and position B and C illustrated no improvement. When the comparison between unaffected scapula and postintervention distance of affected shoulder was performed, there was no significant difference between the groups as illustrated in Table 3. The Fugl-Meyer scores for UE improved significantly in both the groups, but no between-group significance could be demonstrated.

Table 3: Comparison of lateral scapular slide distance (unaffected side versus affected side – post intervention values)

Discussion

The current study aimed to evaluate the effect of scapular PNF-hold relax technique on shoulder pain, ROM, scapular position, and UE function in patients with hemiplegia. The gender distribution observed in this study (percentage of male patients: 60%) matched with that presented in a 2013 report of global burden of stroke which showed that 57.79% of stroke patients were male.[¹⁵] The mean age of all the patients was 56.06 years, 55.73 years for experimental group and 56.40 for control group.

A group of researchers questioned the validity of VAS in stroke patients.[¹⁶] They exhibited the inability of stroke patients to complete the scales with correct pattern and accuracy. However, in this study, VAS was used with confidence because any ambiguity regarding validity was ruled out by excluding the patients with cognitive impairment.

Conventional TENS has demonstrated the positive effects on spasticity, reflex hyperexcitability occurring after stroke.[¹⁷¹⁸] The probable mechanisms underlying this effect are activation of large diameter afferent nerve fibers, modulating the interneuron activities in several spinal segments, which then triggers the inhibition of the activities of presynaptic nerve, or alternatively, it can act through continuous somatosensory stimulation leading to the insensitivity to prolonged excitation accompanied by lower corticomotor neuron excitability.[¹⁷]

PNF has been proven to produce analgesic effects through gate control mechanism.[¹⁹] This mechanism comes into play whenever there occurs any competition between 2 kinds of stimuli, pain and pressure in our case. It is known that nociceptors transmit the pain stimulus either through unmyelinated C fibers or through small myelinated A-delta fibers, and these pain and pressure stimuli relay onto the same region at spinal level. Pressure and proprioceptive inputs (produced by the PNF techniques) make it to the spinal level and inhibit the entry and transmission of pain signals. However, in the current study, the comparison of VAS scores between the 2 groups was not statistically significant implying no benefit of addition of scapular PNF on poststroke shoulder pain. Results of a similar study done by Balc et al.[²⁰] to examine the effectiveness of single session of scapular PNF in patients with adhesive capsulitis resembled very much to that of the current study. One possible explanation for this could be that the structures involved in most common shoulder pathologies poststroke, i.e., adhesive capsulitis and rotator cuff muscle strain[⁵] were not specifically addressed by the scapular PNF techniques administered.

The analgesic effect of TENS not only relieves pain that might occur during the movement but it also corrects the derangement created by inhibition of muscle function developed as a response to pain. The reduction in spasticity and increase in flexibility following the passive conventional exercises also led to the gain in shoulder ROM.

There is agreement for the concept that says the PNF enhances ROM, but the mechanisms illustrated by two groups of researchers are not congruent. Shimura and Kasai[²¹] advocated for the factors such as increment in the excitability and decrease in response time to be responsible for postinterventional increase in ROM while Hindle et al.[¹⁹] proposed the mechanisms such as reduction in the excitability of Golgi tendon organ and induction of relaxation of muscles to lie behind the process of ROM improvement. Single session of scapular PNF has shown to be effective in improving the shoulder ROM – flexion and abduction.[²⁰] Although the techniques administered in above-quoted study were rhythmic initiation and repeated contractions, the pattern of the PNF was similar, i.e., anterior elevation and posterior depression. Another mechanism explained for the increase in ROM relies on the firing of the Golgi tendon organ to cause reflexive muscle relaxation.[¹⁴]

The reluctance of rotation ROM to the therapy can be explained by the analysis of pathologies underlying poststroke shoulder pain. Major contributors of shoulder pathology poststroke were diagnosed to be adhesive capsulitis and rotator cuff injuries.[⁵²²] Adhesive capsulitis involves inflammatory changes in the capsule that surrounds the shoulder joint leading to joint movement restriction. Limitation in passive internal and external rotation ROM has been attributed to capsular pathology.[²³²⁴²⁵] The presence of capsular pathology may have prevented the improvements that could occur following the treatments as in flexion and abduction ROM. The development of spasticity in muscles surrounding shoulder joint leads to pain and restriction of ROM. Most common muscles to undergo spasticity are subscapularis and pectoralis major; this increased tone would have limited external rotation.[²²] The intervention in the current study was not targeted either to capsule or to subscapularis muscle, hence not having effect over these structures.

TENS has been shown to be effective in awareness of proprioceptive sense,[²⁶] it might have aided to the correction of scapular alignment together with other exercises and scapular PNF. Stretching and ROM exercises exerted their effect by enhancing the flexibility of the surrounding muscles. Curtis and Roush[²⁷] demonstrated the correlation to be most for position A and B, and maximum error was found to be at position C. Furthermore, keeping in mind that the scapular PNF was given in the neutral position of shoulder at 0° of abduction and muscles got trained at position similar to position A of LSST, these factors might have led to such results as this study assessed the static alignment of scapula rather than dynamic positioning.

The comparison of postintervention distances on affected side with those on unaffected side gave insignificant results denoting that the position of scapula was similar. The mismatch between ipsilateral and contralateral comparisons points out to the possibilities of the contralateral scapula to have developed dyskinesis over a period of time following cerebrovascular accident; hence, no significant difference could be seen. This very hypothesis of the development of scapular alignment on unaffected side is supported one of the studies which sought to investigate the association between poststroke shoulder pain, scapular kinematics, and shoulder proprioception.[²⁸]

The results obtained in functional outcome mimicked the changes observed in VAS and ROM scores. Lee et al.[²⁹] illustrated the association between pain and function and had shown the beneficial effect of performing exercises in PNF patterns on pain and function. Structures surrounding scapula and shoulder joint do not act efficiently after the damage caused by stroke; restoration of functions of those structures is of utmost importance to have proper shoulder complex function. This restoration is aided by various PNF techniques by normalizing tone and by improving blood circulation.[²⁹] Magarey and Jones[⁸] presented the relation between pain and altered timing of contraction in stabilizing muscles and that inhibition of muscles as a nonspecific response to any painful condition of shoulder disorganizes the normal firing pattern and hampers the ability to produce torque and to stabilize the scapula. They support the theory of training in the pattern of force couples (synergy) rather than in isolation and beneficial effect of using tactile, verbal, weight bearing, and movement-oriented cues, and both of these features were utilized in the PNF techniques administered.[⁸] Hence, the improvement achieved in both the groups can be attributed to the reduction in level of shoulder pain, increase in proximal muscle strength, and gain in shoulder ROM as a result of conventional treatment and scapular PNF.

Few limitations that strived in this study were (1) shoulder muscle assessment was not performed specifically; shoulder muscle pathology might have influenced the outcomes assessed in this study, and (2) absence of follow-up eliminated the chance of examining whether any between-group differences appeared in a longer run. PNF methods facilitating lateral/upward rotation movement or corresponding muscles need to be researched as kinematic studies have shown that upward rotation is the most impaired scapular motion following stroke, and this impairment further causes secondary impairments in and around the scapula. PNF-hold relax technique targeting subscapularis and pectoralis major in patients with poststroke shoulder pain needs to be researched upon for its effect on internal and external ROM. The effect of combination of scapular PNF and UE PNF on shoulder complex function demands to be studied as it seeks to assess the effect of training UE as a whole.

Conclusion

It can be stated that scapular PNF is a vital component of the poststroke shoulder pain rehabilitation protocol. Scapular PNF helps in alleviating the shoulder pain, in increasing shoulder ROM, strengthening of scapular and proximal muscles of UE, and in correcting the alignment of scapula improving the function of UE. However, the beneficial effects could not be found pertaining to the joint capsule and muscles such as subscapularis and pectoralis major. The improvement seen in scapular position only in position A demonstrated that the treatment effects did not transfer to any positions other than in which the PNF was administered.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

Acknowledgement

The authors of the study express their sincere thanks to the Principal of the Institute of Physiotherapy. We would also like to thank the tertiary care hospital management for giving permission to carry out the study and also the patients for their willingness to participate.