Assessment of shoulder proprioception in patients with chronic mechanical cervical pain: A comparative study

1. Introduction

Chronic cervical pain is a highly prevalent (42–67%) disabling problem among young adults worldwide, leading to reduced quality of life, reduced work productivity and a considerable economic cost [1, 2, 3]. Mechanical neck pain refers to a pain of non-specified etiology with a prevalence of 60 to 70% in general population. It could be associated with or without pain in the upper limb and may or may not interfere with activities of daily living (ADL) [4, 5].

Proprioception plays a crucial role in the sensori-motor control of human movement; which is essential in all ADL, exercises and sports [6]. Proprioception is described as a combination of joint position sense (JPS); the ability of a person to identify the position of a limb in space, kinesthesia, sense of force, and velocity [7, 8] Proprioceptive feedback contributes to the regulation of muscle contraction, movement acuity, joint stability, the maintenance of optimal body alignment, coordination and balance [9, 10, 11].

The central nervous system (CNS) utilizes the proprioceptive feedback in building body schema and central awareness/perception for each segment within the body. This central awareness is a key for executing a selective controlled movement. Consequently, impaired proprioception can negatively impact perception, selective movement control, postural stability, and cause several recurrent injuries [11, 12, 13, 14].

For the shoulder joint, the importance of proprioceptive feedback comes from the fact that this joint is inherently unstable and provides a wide movement range. Proprioception acuity, in conjunction with neuromuscular control elements, is critical for shoulder stability and controlled mobility [8, 15] as well as accuracy of hand movement during functional tasks of upper extremities [16]. Several studies have investigated the relationship of impaired shoulder proprioception with its stability and mobility, and with functional limitations [17, 18].

The relation between neck pain and shoulder dysfunction is addressed from different prospective, and attributed to anatomical, biomechanical and neurological connections between these two inter-related segments [19, 22].

Chronic non-specified neck pain can possibly change biomechanical relations, and alter kinetics and kinematics of scapula and shoulder. Furthermore, neck pain plays a role in altering patterns of muscle activation of the shoulder complex, causing its pain and dysfunction in the long term [23, 24].

Studies have shown that chronic neck pain is accompanied by reduced proprioceptive acuity in elbow [25] and shoulder [26] joints. However, those studies were conducted on patients with whiplash-injures [25, 26]. Although the CMCP is a prevalent problem in young adults, to our knowledge, only one study investigated the influence of CMCP on the acuity of shoulder proprioception in young females, and revealed an impaired proprioception at shoulder, elbow and hand joints measured by a digital inclinometer sensor [27]. To the best of our knowledge, arm dominance and rotation direction effects on shoulder proprioception were not previously addressed in the studies of neck pain.

Therefore, the current study was conducted to investigate the impact of CMCP on shoulder proprioception in young adults compared with matched healthy subjects. Additionally, the effects of arm dominance and rotation direction on shoulder proprioception were addressed in our work.

2. Material and methods

Subject characteristics showed no significant difference between groups (Table 1). Mixed MANOVA revealed that there was no significant interaction of group, arm dominance and rotation direction ( F (1, 78) = 0.02, p = 0.87). However, there was a significant main effect of group ( F (1, 78) = 146.37, p = 0.001), arm dominance ( F (1, 78) = 14.64, p = 0.001), and rotation direction ( F (1, 78) = 10.45, p = 0.002). The AAE was significantly increased in DS and NDS at both IR and ER in the CMCP group compared with the NC one (Table 2). A significant difference between DS and NDS at IR and ER was only detected in the CMCP (Table 2). Further, a significant difference in the AAE of the ER on both DS and NDS was only detected in the CMCP (Table 3).

This work demonstrated that young adults with CMCP have a reduced acuity of shoulder proprioception, particularly in their dominant shoulder and at the external rotation range, compared to healthy subjects. The results of CMCP group showed a significant reduction in shoulder AJPS for both IR and ER on both DS and NDS when compared to NC group. Only in the patient group, there was a significant difference in the AJPS between DS and NDS and between ER and IR ranges, to our knowledge, those findings have not been previously reported in CMCP.

The joint repositioning test is reported as an efficient method to explore the acuity of proprioception [6] and enables exploration of hemispheric asymmetries in sensorimotor abilities [36]. For that reason, the angular error of shoulder AJPS was measured on both DS and NDS in the present work using an objective and highly reliable system; the isokinetic dynamometer (BS3-ID) [31]. Shoulder rotations; external and internal were particularly measured and compared in this work because of their significance in detecting shoulder proprioceptive deficits and thus shoulder instability [16, 30, 34, 37]. The isokinetic dynamometer provided a stable and precise arm position during the shoulder AJPS testing, which consequently reduced the tension of rotator cuff and scapular muscles. This proper setting eliminates the impact of scapular abnormalities on measurements and ensures a good sensitivity of measuring AJPS for shoulder rotations [34].

A reasonable explanation of the reduced shoulder AJPS in this work, might be based on the understanding of biomechanical and neurological basis. Normally, the CNS utilizes the sensory information about the head and neck positions when interpreting the position of the upper limb. Therefore, an altered input from neck region may affect the sensory information to the CNS and consequently impair the awareness of joint position proximally at shoulder region [27, 38, 39] or more distally at elbow [27, 40] and hand [27].

Neck pain is found to significantly alter scapular and shoulder alignment [38, 39] and change the acuity of their proprioception and awareness [26, 41]. Moreover, the neurophysiological studies proved the influence of chronic pain on changing the level of proprioception through affecting the memory of muscle, joint sense, the activation of muscle spindle and the excitability of the afferent nerves [8, 42, 43, 44].

The results of the current study can be supported by the work of Abichandani and Parka [27], which also reported an impaired acuity of shoulder proprioception in CMCP. In their work, active reposition test was only conducted on young females at 30 ∘ of shoulder adduction, from a starting position of 90 ∘ shoulder flexion, at supine lying position using a digital inclinometer sensor.

Another study conducted by Sandlund et al. [26] also revealed a reduced acuity of shoulder proprioception, however, their work was conducted on patients with whiplash injuries using an electromagnetic tracker system with different setting and target shoulder angle.

The reduced AJPS in young adults with CMCP may have a particular clinical value regarding the shoulder stability-mobility function in this population. Shoulder stability and mobility are correlated for providing the optimum function of upper extremities. Proprioceptive dysfunction would interfere with shoulder stability and selective motor control during different activities [11, 12, 13, 14]. Further, impaired shoulder proprioception in neck pain plays an important role in influencing the acuity of goal directed arm movement and consequently producing uncontrolled movement [45].

The reduced AJPS would indicate impaired mechanoreceptors of passive stabilizers of shoulder which disturb the balanced stability-mobility function, and dominates a mechanism of “stability over mobility”. In this mechanism, the demands of stability are provided while the shoulder mobility patterns are altered and limited secondary to the developed adaptive structural changes within and around the shoulder joint. These changes disturb the neuromuscular control of shoulder complex which causes further impairments of shoulder function and increases the susceptibility to frozen shoulder and risk of injury [34, 46].

Another finding of the current study was the significantly reduced shoulder AJPS on the DS compared to the NDS, that was only observed in the CMCP group. To our knowledge, no study investigated the dominance effect on shoulder proprioception in CMCP. Many studies showed no dominance effect on the shoulder proprioception in healthy subjects [7, 16, 47, 48, 49], which matched the results of NC group in the present work. Other studies revealed a discrepancy in the perception of proprioceptively determined dynamic position sense of upper limbs, which was explained by the difference between both cerebral hemispheres in utilizing sensory information for the control of movements [36, 50, 51, 52]. The right cerebral hemisphere/non-dominant (left) arm mainly depends on either position [51] or dynamic proprioceptive information [36, 50], however, the left hemisphere/dominant (right) arm is more dependent on visual feedback [52] for the processing and execution of controlled movement.

In the present work, all subjects in both groups were right-handed (left dominant cerebral hemisphere), properly positioned and blindfolded during the test, which made the testing procedure highly demanding on the sensitivity of shoulder proprioception.

Normally, the dominant arm has various advantages of the motor output of (e.g. strength, speed and time consistency) than non-dominant side during motor performance of rhythmic coordinated movements of upper limbs [50]. Thus, the remarkable reduction of dominant shoulder AJPS in this work, would clinically signify an adequate examination of the dominant arm stability and motor performance during coordinated movement in young population with CMCP.

Studies have also reported the extensive use of dominant arm more than the non-dominant one during ADL significantly alters muscular activation, changes the alignment and kinematics of shoulder girdle [38, 53, 54] and consequently reduces the perception level [8, 38, 39, 44]. Commonly, short and overactive pectorals and latissimus dorsi together with inefficient trapezius muscle reduce the firing of serratus anterior muscle and contribute to the excess scapular protraction [38, 53, 54] which causes the multidirectional instability of the glenohumeral joint [55].

Adaptive shortening or tightness of pectoralis minor changes scapular kinematics and alignment into anterior tilting, downward and internal rotations, restricts both scapular upward and external rotations, and humeral external rotation, and subsequently disturb scapulo-humeral rhythm required during arm elevation and causes further pain at shoulder and/or neck regions [56, 57].

Although muscle flexibility and activation patterns were not measured in our study, the facts mentioned above, could be considered when explaining the reduced acuity of proprioception.

Another observation in this work was the remarkable reduction of AJPS for shoulder ER compared to IR, which was only detected in the CMCP group. Some studies reported defective proprioception in ER than IR during AJPS [26, 34, 35, 58], however, comparing those results to ours may not be applicable because of the differences in sampling selection, purpose and measurements. In 2016, Fabis et al. [34] reported that the significant difference between AJPS for shoulder ER and IR, is an important indicator for proprioceptive deficit, helping to identify shoulders at risk especially in overhead activities. According to our results, young adults with CMCP might develop a risk of shoulder injury that should be considered during the management of this population.

5. Conclusion

Chronic mechanical cervical pain can significantly impair shoulder active sense of position in young adults with CMCP, particularly on the dominant side and in external rotation range, which was not previously reported in this population. This study has a significant clinical implication that could be the necessity of adequate and careful examination of shoulder proprioception, particularly on the dominant side, for the early detection of shoulders at risk, to eliminate the possibility of shoulder instability and/or injury in young population with CMCP.