Neck Position Affects Scapular Orientation in a Posture of Simulated Rugby Tackling

Objective: To investigate the effects of head position on scapular orientation in a posture of simulated rugby tackling. Design: Laboratory experimental study. Methods: Twenty-nine healthy young men lay on the edge of a wooden rigid bed in the prone position with their dominant arm free. The experimental arm movement task was conducted in four head positions (2 neck bending x 2 neck rotation) with maximum ranges of direction: the dominant arm was rotated from an intermediate position to maximum external rotation at 90° shoulder abduction with 90° elbow flexion while maintaining each neck position. During the tasks, dynamic scapular orientations were measured with an electromagnetic sensor system. Results: In total, 348 experimental trials were included in the analyses. Two-way repeated-measures analysis of variance demonstrated that the direction of neck bending and the side of neck rotation relative to the arm movement significantly affected the scapular orientation. The scapular tilting angle was significant during neck rotation ipsilateral to the arm movement (mean difference, 11°). The scapular upward rotation angle was higher during neck rotation contralateral than ipsilateral rotation to the arm movement (mean difference, 2.5°) regardless of the neck bending position. The scapular external rotation angle was significant during neck rotation ipsilateral to the arm movement (mean difference, 5.5°). Conclusions: The neck position affects the scapular orientation in the prone position. Neck flexion with rotation contralateral to the arm movement represents an anteriorly tilted and internally rotated scapula orientation, which may increase the risk of shoulder injury such as dislocation.


Introduction
The arm orientation has been recognized as a substantial factor of the shoulder dislocation from clinical experiences. However, the previous cadaveric studies of the dislocated cases failed to clarify precise mechanisms of dislocation 1) . During the competition of rugby, which is one of the most popular collision sports worldwide, the shoulder dislocation develops frequently by tackling, so that the study of rugby would provide useful information to reveal the mechanisms of shoulder dislocation in a real-world settings [2][3][4][5] . During competitive rugby, the most frequent mechanism of shoulder dislocation is tackling. Several studies in which rugby tackling was analyzed using video recordings 6,7) showed that anterior shoulder dislocation may occur when the tackler's approach fails and his arm is forcibly moved in the posterior direction at the time of impact with the ball carrier. In this situation, the affected shoulder is subjected to a combination of abduction, external rotation, and horizontal abduction during contact.
A recent video analysis showed an alternative type of tackling-induced injury characterized by tackler's shoulder with a lowered head in front of the opponent at the time of impact, which was regarded generally as an inappropriate posture 7) . This lowered head appears to increase the joint position error of the arm, which may be caused by a change in the gaze direction, disrupted integration of sensory coordinates, or distraction from head and neck movements 8) . This type of tackle has been reproduced in the experimental setting using a three-dimensional motion capture system, and different shoulder orientations were also evident 9) . The findings of previous studies indicate that the tackler's inappropriate posture with a lowered and contralaterally rotated neck influences the glenohumeral joint via the scapula orientation, which seems to be a primary factor in the cause of anterior shoulder dislocation. These findings seem useful for speculation of the mechanisms of shoulder dislocation during rugby tackling; however, the studies focused on the humerothoracic angle instead of the glenohumeral angle. Thus, the precise mechanisms of dislocation remain unknown because the methods of these studies provided no information about the orientation of the scapula. Investigation of the scapular orientation may facilitate the establishment of a preventive strategy for shoulder dislocation during tackling.
Several researchers have recently used an electromagnetic sensor system to measure the scapular orientation [10][11][12][13] . Past reports have demonstrated that neck flexion induces scapular anterior tilting and elevation, which may have a negative effect on shoulder stability [10][11][12] . The effects of the neck and trunk positions relative to the scapular orientation have been shown in various models using this system. However, to the best of our knowledge, no published literature has addressed the effect of the neck position, especially rotation, on scapular orientation in the prone position.
The present study was performed to elucidate the effects of neck bending and rotation on scapular orientation during arm movements in a prone position that simulates a tackling posture and to determine the neck position that is associated with a risk of shoulder dislocation. We hypothesized that rotation of the neck has an additive effect on scapular orientation and that neck flexion with contralateral rotation causes the worst scapular orientation.

Material and methods
Twenty-nine healthy young men (age, 28.0 ± 5.4 y; height, 172.3 ± 6.5 cm; weight, 70.6 ± 8.7 kg) with no history of neck, shoulder, or elbow pathology or pain participated in the present study. All subjects provided written informed consent to participate in the study. This research was approved by the ethics review board of our institute (No. 2016024).

Study design
The subjects lay on the edge of a wooden rigid bed in the prone position with their dominant arm (right in all cases) free to allow performance of tasks without any obstacles. To determine whether the head and neck position affects scapular orientation, an experimental arm movement task was conducted in four neck positions with maximum ranges of direction: (1) combined extension with rotation ipsilateral to the arm movement (Figure 1a  to avoid the influences of fatigue and learning effects. Before the trials, the subjects were instructed and encouraged to perform the humeral movement task by rotating the dominant arm from an intermediate position to maximum external rotation at 90º shoulder abduction with 90º elbow flexion while maintaining each neck position in the prone position. To maintain the height of the elbow relative to the thorax during the task, the examiner assisted the subject in keeping the center of the elbow movements consistent during arm rotation in all tests. Clinically, this simulated a tackling posture applied to the shoulder with the thorax and humerus in the same position, with only the position of the scapula changing. Each task was performed for a standardized count of 2 seconds to ensure a consistent speed, and the subject returned to the initial position during the following 2 seconds. Five trials were performed to allow for assessment of the reproducibility of the results, and the middle of the five trials (the third trial in each task) was analyzed.

Kinematic recording and data reduction
The spatial positions of the neck, thorax, scapula, and humerus were measured using the Liberty 8-channel electromagnetic motion capture system (Polhemus; Colchester, VT, USA). Data were collected at a sampling rate of 120 Hz. The transmitter, which generates a low-frequency electromagnetic field, was set on a rigid wooden frame, and a global coordinate system was established. The landmarks were chosen in accordance with the International Society of Biomechanics (ISB) recommendations (Wu et al, 2005): the C7 and T8 spinous processes, the sternoclavicular joint, and the xiphoid process were the thoracic landmarks; the midpoint of the humerus and the medial/lateral epicondyles were the humeral landmarks; the acromial angle, base of the spine, and inferior angle were the scapular landmarks; and the C7 spinous process and parietal region of the head were the cervical landmarks. The seven wired electromagnetic sensors were attached to these body landmarks, and a stylus with an embedded electromagnetic sensor was used to digitize the landmark positions of each segment (thorax, humerus, and scapula).
The motion of the body segments in three dimen-sions was described using three sequential Euler angle rotations to express the orientations of the scapula and humerus as distal segments relative to the thorax as the proximal segment, in accordance with the ISB recommendations 14) . In short, the origin of the scapular rotation was coincident with the Angulus Acromialis (AA), Z axis (tilting) was defined as the line connecting AA and Trigonum Scapulae (TS), X axis (upward rotation) was defined as the line perpendicular to the plane formed by AA, TS, and Angulus Inferior, and Y axis (external rotation) was defined as the common line perpendicular to the X-and Z-axis. The scapular angles [posterior(+)/anterior(-) tilting, upward(+)/downward(-) rotation, and external(+)/internal rotation(-)] were calculated at selected humeral rotation angles during the ascending phase of each task using a custom code in MATLAB (MathWorks, Natick, MA, USA). To avoid the effects of arm movement on scapular orientation at the end-range of each motion, we used the data from an intermediate position to external rotation to 70º in each task for the following analysis. A past study demonstrated that the system used in the present study ensured an angular orientation accuracy of 1.3°1 5) . The root mean square error due to skin motion artifact was 2.0º to 9.4° when the humeral elevation was <120° 15,16.

Statistical analysis
The trial-to-trial reliability statistics calculated for the scapular kinematic measurements at humeral rotation from 0º to 70° were the intraclass correlation coefficient (ICC)(1,3) and standard error of measurement (SEM). The reliability among different examiners, ICC(2,1) or ICC(3,1), was not tested in this study. The main analysis was performed to compare the scapular orientation during arm movement and thus elucidate the effects of various neck positions. Comparisons of the scapular orientation among the tasks were performed with two-way repeated-measures analysis of variance with 2 x 2 factors: bending (extension, flexion) and rotation (ipsilateral, contralateral to the arm movement) of the neck. A p value of <0.05 was considered statistically significant, and all tests were two-sided. The data analyses were conducted with SPSS software for Macintosh, v. 21.0 (IBM Corp., Armonk, NY, USA).

Results
The variables from all 348 experimental trials among the 29 subjects were included in the analyses, and these data are summarized in Table 1. The ICC (and SEM) for trial-to-trial reliability in each task ranged from 0.95 to 0.98 (SEM, 1.14-1.78) for scapular tilting, from 0.96 to 0.98 (SEM, 0.80-1.38) for scapular upward rotation, and from 0.97 to 0.99 (SEM, 0.90-1.60) for scapular external rotation ( Table 2). Before the main analyses, we assessed correlations with the scapular orientations among all tasks. Scatter plots and linear correlations (Figure 2) showed that scapular tilting was significantly correlated with scapular external rotation (r2 = 0.23, p < 0.01) and that scapular upward rotation was also correlated with scapular external rotation (r2 = 0.13, p < 0.01). The estimated marginal means of the scapular orientations at each angle of arm movement are summarized in Figure 3.
In the main analysis, two-way repeated-measures analysis of variance revealed the effects of neck bending (extension/flexion) and/or neck rotation (ipsi-/contra-lateral) to the scapular orientation during the task (Figure 4). The scapular tilting angle relative to the thorax segment was higher during neck extension (p < 0.001), and this finding was more significant during neck rotation ipsilateral to the arm movement (mean difference, 11°; p < 0.001) (Figure 4a). The scapular upward rotation angle relative to the thorax segment was higher during neck rotation contra-   lateral than ipsilateral to the arm movement (p < 0.001), and the mean difference of the angle was about 2.5° regardless of the neck bending position (Figure 4b). The scapular external rotation angle relative to the thorax segment was higher during neck extension (p < 0.001), and this was more significant during neck rotation ipsilateral to the arm movement (mean difference, 5.5°; p < 0.001) (Figure 4c).

Discussion and implications
We investigated the effects of the neck position on the scapular orientation during humeral rotation in the prone position with 90° shoulder abduction and demonstrated some important findings. In the main analysis, two-way repeated-measures analysis of variance demonstrated that both factors [the neck bending directions (extension/flexion) and the side of the neck rotation relative to the arm movement] independently affected the scapular orientation ( Figure 4). First, the scapular posterior tilting angle was higher during neck extension than flexion (p < 0.001), and this finding was more significant in neck rotation ipsilateral to the arm movement. The largest mean difference in the angle among the neck positions was about 12° between neck extension with rotation ipsilateral to the arm movement and neck flexion with rotation contralateral to the arm movement.
Second, the scapular upward rotation angle during the task was higher during neck rotation contralateral than ipsilateral to the arm movement (p < 0.001), and the mean difference in the angle was about 2.5° regardless of the direction of neck bending. These results are consistent with a past study in which the scapular upward rotation angle was affected by neck rotation but not by neck bending 12) .
Third, the scapular external rotation angle was higher during neck extension than flexion (p < 0.001), and this finding was more significant during neck rotation ipsilateral to the arm movement (p <  To summarize these results, we found that the most striking differences in the scapular orientations occurred between neck extension with rotation ipsilateral to the arm movement and neck flexion with rotation contralateral to the arm movement. The former represents maximum posterior tilting, upward rotation, and external rotation, whereas the latter represents the minimum values of the scapular orientations; that is to say, the "winged scapula" position. Past studies have indicated that the posture involving scapular anterior tilting and glenoid anteversion appears to influence (increase) the shearing force on the glenohumeral joint as well as the loading to the glenohumeral ligament via the scapular orientation [17][18][19] . In addition, an inadequate position of the scapula may lead to dysfunction of the scapular muscles, which also affects scapular stabilization 17) . Both of these factors are important in anterior shoulder dislocation. These issues might help to explain why tackling with a lowered head leads to shoulder dislocation and that to prevent shoulder dislocation, neck flexion with rotation contralateral to the arm movement is not recommended in rugby tackling.
In the present study, we focused our investigation on the cooperative movement between the neck and scapulae during arm movements. The scapular orientation is mainly operated by five periscapular muscles; the levator scapulae, the upper and middle trapezius, the lower trapezius, the rhomboids, and the serratus anterior. These muscles are essential for stabilizing the proper orientation of the scapula and that weakness of these muscles may lead to improper orientation of the scapula during arm movement 20) .
The origin of the levator scapulae is the C1-4 transverse process on the ipsilateral side of the muscle, and its insertion is at the superior angle of the scapula 21) . Whereas, the origin of the upper trapezius is the cranium to C7 Spinal process on the ipsilateral side of the muscle, and its insertion is at the acromion 21) . Previous studies have shown that the former acts to elevates and externally rotates the scapula, while the latter acts to elevates the scapula and rotates it upward when the cervical spine is fixed 21,22) . These reports, together with the present results, suggest that the activity of the levator scapulae tend to be high in neck extension, and it seems to be highest during neck extension with rotation ipsilateral to the arm movement and lowest during neck flexion with rotation contralateral to the arm movement. Contrary to the levator scapulae, the activity of the upper trapezius may be low in all neck positions during the task due to its anatomic characteristics, and this is suggested by a past report in which electromyogram was investigated in the prone position 23) . Thus, it seems reasonable to conclude that the levator scapulae is more important than the upper trapezius for maintaining an ideal shoulder position, while both muscles run across the scapula and cervical vertebrae anatomically. Regarding to the other two periscapular muscles that run across the scapula and thorax; the lower trapezius and the serratus anterior, both of these muscles are believed to be important for stabilization of the scapula and facilitate scapular posterior tilting. Thus, both of the muscles may contribute to maintaining the neck extension position through scapular stabilization during arm movements.
To apply our findings to rugby tackling, neck flexion with rotation contralateral to the side of the impacted shoulder may increase the risk of shoulder dislocation. Muscle strengthening exercises of the levator scapulae, lower trapezius, and serratus anterior may help to avoid improper orientation of the scapula ( Figure 5). With respect to a possible mechanism of shoulder dislocation, identification of the positional relationship between the scapula and the humerus is essential to determine the shearing and compression forces on the glenohumeral joint. Thus, we believe that addressing the scapular orientation during sports-specific movements is an important issue, as shown in the present study.

Limitations
Despite the important findings of this study, it also has several limitations. First, the position applied in the present study was not a true position in rugby tackling. In many images of rugby tackling, the torso is prone like but not parallel to horizontal. The difference may also affects the activity of the periscapular muscles during the tasks. Thus, further justification is needed for these alterations to truly simulate rugby tackling. Second, the muscle activities during the task were not provided from the present study. Actually, we have measured them by using surface electromyogram, but those were omitted from our results, because of insufficiency of data accuracy. A further clinical study with a larger number of subjects is needed to confirm our findings.

Conclusions
The present study indicates that the neck position affects the scapular orientation when the subject is lying prone, which simulates a tackling position. Neck flexion with contralateral rotation to the impacted shoulder represents an anteriorly tilted and internally rotated scapula orientation, and this may increase the risk of shoulder injury such as dislocation.