Yoann Blache
email: yoann.blache@univ-lyon1.fr

Thomas Creveaux

Raphaël Dumas

Laurence Chèze

Isabelle Rogowski

Glenohumeral contact force during flat and topspin tennis forehand drives

Keywords: Glenohumeral contact force, shoulder, musculoskeletal model, racket sports, anterior-superior glenoid shearing force

The primary role of the shoulder joint in tennis forehand drive is at the expense of the loadings undergone by this joint. Nevertheless, few studies investigated glenohumeral (GH) contact forces during forehand drives. The aim of this study was to investigate GH compressive and shearing forces during the flat and topspin forehand drives in advanced tennis players. 3D kinematics of flat and topspin forehand drives of 11 advanced tennis players were recorded. The Delft Shoulder and Elbow musculoskeletal model was implemented to assess the magnitude and orientation of GH contact forces during the forehand drives. The results showed no differences in magnitude and orientation of GH contact forces between the flat and topspin forehand drives. The estimated maximal GH contact force during the forward swing phase was 3573 ± 1383 N, which was on average 1.25 time greater than during the follow-through phase, and 5.8 times greater than during the backswing phase. Regardless the phase of the forehand drive, GH contact forces pointed toward the anterior-superior part of the glenoid therefore standing for shearing forces.

Knowledge of GH contact forces during real sport tasks performed at high velocity may improve the understanding of various sport-specific adaptations and causative factors for shoulder problems.

Introduction

Playing tennis applies repeated high loads onto the upper limb joints, especially onto the shoulder complex [START_REF] Elliott | Technique effects on upper limb loading in the tennis serve[END_REF]. If the serve places the tennis player at the highest risk for impingements at the shoulder [START_REF] Charbonnier | Shoulder motion during tennis serve: dynamic and radiological evaluation based on motion capture and magnetic resonance imaging[END_REF], repeated powerful forehand drives may also be a cause of shoulder problems.

The achievement of a forehand drive requires three successive phases: a slow backswing to place the body at an optimal pose before the drive, a rapid forward swing to accelerate the racket head for impact, and a follow-through to slowdown the upper limb-racket complex [START_REF] Ryu | An electromyographic analysis of shoulder function in tennis players[END_REF]. Two techniques of forehand drives are mainly used by advanced tennis players: the flat and topspin. The main difference between the two techniques is the racket path during the forward swing. For the flat forehand drive, the racket is mainly moved horizontally, while, for the topspin shot, the racket is first moved downward, then upward until ball impact. Such differences generate a higher vertical velocity of the racket head at impact for topspin than for flat forehand drives [START_REF] Takahashi | The role of upper limb segment rotations in the development of spin in the tennis forehand[END_REF]. Nevertheless, whatever the technique used and according to the kinetic chain concept described by [START_REF] Elliott | A biomechanical comparison of the topspin and backspin forehand approach shots in tennis[END_REF], the racket head velocity at impact is a result of the cumulative force production at successive body joints. In this context, shoulder motions have a high contribution in the total force production. [START_REF] Takahashi | The role of upper limb segment rotations in the development of spin in the tennis forehand[END_REF] indeed observed that the shoulder complex accounts for 60% of the upper limb contribution to the racket head velocity during the forward swing phase. The role of the shoulder seems to remain similar whatever the forehand drive technique, i.e. flat, topspin or lob [START_REF] Takahashi | The role of upper limb segment rotations in the development of spin in the tennis forehand[END_REF], the shot velocity [START_REF] Seeley | Tennis forehand kinematics change as post-impact ball speed is altered[END_REF], or the skill level [START_REF] Landlinger | Kinematic differences of elite and high-performance tennis players in the cross court and down the line forehand[END_REF].

The primary contribution of the shoulder joint in the racket velocity generation is at the expense of the loadings undergone by this joint. Indeed, the great shoulder joint amplitude and velocity required during the forward swing and follow through phases, i.e. humeral horizontal adduction and internal rotation [START_REF] Marshall | Long-axis rotation: the missing link in proximal-todistal segmental sequencing[END_REF], may lead to high shoulder contact forces. To our knowledge, few studies investigated the loading undergone by the shoulder during forehand drives. Two studies investigated the shoulder loadings by computing the net joint moment/power at the humero-thoracic joint [START_REF] Bahamonde | Kinetics of the upper extremity in the open and square stance tennis forehand[END_REF]Creveaux, Dumas, Cheze, Mace, & Rogowski, 2013a). [START_REF] Bahamonde | Kinetics of the upper extremity in the open and square stance tennis forehand[END_REF] observed that the horizontal adduction component was the greatest shoulder moment during the forehand drive. Another study investigated the consequences of shoulder loadings during forehand drive by estimating the distance between different shoulder structures [START_REF] Ladermann | Kinematics of the shoulder joint in tennis players[END_REF]. They observed a decrease in the humeroglenoid distance that led, in 29% of the cases, to an anterior-superior humero-glenoid impingement; namely an impingement of the deep surface of the subscapularis tendon and the reflection pulley at the anterior-superior part of the glenoid cavity [START_REF] Gerber | Impingement of the deep surface of the subscapularis tendon and the reflection pulley on the anterosuperior glenoid rim: a preliminary report[END_REF].

Although these studies give a first estimation of the shoulder loadings during the forehand drive, few information are available on the contact forces at the glenohumeral joint.

Contact forces take into consideration both the external forces and the muscle forces acting on the joint [START_REF] Steele | Compressive tibiofemoral force during crouch gait[END_REF]. Contact forces are usually hard to estimate by experimental assessments since based on invasive methods such as instrumented prosthesis [START_REF] Nikooyan | Validation of the Delft Shoulder and Elbow Model using in-vivo glenohumeral joint contact forces[END_REF]. Musculoskeletal models therefore offer a promising alternative. Indeed, they make it possible to estimate muscle forces; then the later can be used in addition to external forces to compute contact forces [START_REF] Prinold | Musculoskeletal shoulder models: a technical review and proposals for research foci[END_REF][START_REF] Quental | Critical analysis of musculoskeletal modelling complexity in multibody biomechanical models of the upper limb[END_REF]. Consequently, musculoskeletal models have been already used to estimate glenohumeral contact forces during wheelchair propulsion [START_REF] Holloway | Linking wheelchair kinetics to glenohumeral joint demand during everyday accessibility activities[END_REF][START_REF] Van Drongelen | Load on the shoulder complex during wheelchair propulsion and weight relief lifting[END_REF][START_REF] Veeger | Load on the shoulder in low intensity wheelchair propulsion[END_REF], driving task [START_REF] Pandis | Shoulder muscle forces during driving: Sudden steering can load the rotator cuff beyond its repair limit[END_REF] or daily life activities [START_REF] Anglin | Glenohumeral contact forces[END_REF]. Consequently, musculoskeletal model may be helpful to better assess glenohumeral contact forces during tennis forehand drives.

The aim of this study was to investigate the contact force at the glenohumeral joint during the flat and topspin forehand drives in advanced tennis players. We hypothesised that contact force magnitude and orientation would be similar for the flat and topspin forehand drives, and different between the three phases of the stroke.

Methods

Participants

After given their informed consent, 11 right-handed male competitive tennis players (Mean ± SD age: 29.1 ± 7.6 years; mass: 69.4 ± 5.6 kg; height: 178 ± 6 cm; tennis experience: 22 ± 7 years; weekly training exposure: 5.1 ± 5.8 h; International Tennis Number: 3) volunteered to participate in this study, which was approved by French Ethics Committee Sud-Est II. The players declared no history of injury in the six months before the study. Six players used a semi-western grip, while the other five a western grip, to hit forehand drive. All players were classified in the advanced level (level 3) according to the International Tennis Number (ITN) classification. This meant that the players were able to hit strong forehand drive with control, depth and spin, and to vary spin. The mass, centre of gravity, swingweight and twistweight, i.e. the moments of inertia around the transversal and perpendicular axis of the racket head plane of each player were measured using a Racket Diagnostic Center (Babolat VS, Lyon, France). Polar moment was calculated by subtracting the twistweight and swingweight (Brody, 1985) (see Figure S1 in the supplementary file for axis definitions).

Instrumentation and data collection

In line with previous study [START_REF] Rogowski | Effects of the racket polar moment of inertia on dominant upper limb joint moments during tennis serve[END_REF], each participant was fitted with 17 reflective markers located on the xiphoid process; incisura jugularis; 7th cervical vertebra; 8th thoracic vertebra; and on the right side, angulus acromialis; acromio-clavicular joint; scapula spine (at 1/3 of the spine from the acromion); inferior and superior scapula angles; distal insertion of the middle deltoid; medial and lateral humeral epicondyles; olecranon; radial and ulnar styloid processes; and 2nd and 5th metacarpal heads. In addition, three reflective markers were stuck on the racket and a reflective tape surrounded the ball. The 3D trajectories of the reflective markers were recorded using an optical motion capture system (Motion Analysis, Motion Analysis Corporation, Santa Rosa, CA, USA) comprising eight digital cameras (sampling frequency: 500 Hz).

Procedure

After a 15-min warm-up, each player performed randomly two series of two sets of six successive crosscourt forehand drives; flat forehand drives were hit during one series, and topspin forehand drives during the second one. The players used their own racket (mass: 334 ± 13 g; centre of gravity measured from the handle racket extremity: 328 ± 8 mm; swingweight: 327 ± 9 g.cm²; twistweight: 343 ± 10 g.cm²; polar moment: 15.7 ± 1 g.cm²).

They were instructed to hit the ball at their own playing velocity in a comfortable way, when using a square stance. All trials were conducted in an indoor acrylic tennis court, which was instrumented with a ball machine (ball velocity: 16.7 m/s; Airmatic 104, Pop-Lob, Bagneux, France) located on the baseline of the opposite tennis court, and with a radar gun (Stalker Pro II, Stalker Radar, Plano, TX, USA) located behind the player to measure ball velocity after the ball impact.

Musculoskeletal model

The Delft Shoulder and Elbow model (van der Helm, 1994) available on OpenSim [START_REF] Delp | OpenSim: open-source software to create and analyze dynamic simulations of movement[END_REF] was used. Briefly, the model was composed of eight segments (ground, thorax, right clavicle, scapula, humerus, ulna, radius and hand). A racket was added to the model to reproduce the forehand drives. The segments were linked by 18 degrees of freedom namely the ground-thorax joint (three translations and three rotations), sterno-clavicular joint (two rotations), acromio-clavicular joint (three rotations), glenohumeral joint (three rotations), elbow (two rotations) and wrist (two rotations). No degree of freedom was allowed between the hand and the racket. The later was placed in the model for each participant according to its position recorded at the beginning of the forehand drives. The 18 degrees of freedom were actuated by 139 muscle lines of action (Figure 1).

Scaling and kinematics

The generic model was scaled for each participant using the position of the reflective markers recorded during the static pose. In addition, the inertia, mass and size of the participants' racket were used for each scaled model. Then, an inverse kinematic procedure was used to obtain the joint angles by minimising the Euclidian distance between the position of the virtual markers and the position of the experimental markers at each sample time. Moreover, an ellipsoid fitted to the semi-right-thorax was implemented with a two-point-on-ellipsoid constraint ensuring the scapula to follow the thoracic curvature throughout the movement [START_REF] Michaud | Thorax ellipsoid optimization based on scapula movements' area improves kinematic reconstruction of the scapula[END_REF]. For further analysis, joint angles were filtered using a zero-lag fourth-order low-pass Butterworth filter with an 8 Hz cut-off frequency. To avoid problems of data filtering through ball impact [START_REF] Knudson | Effect of endpoint conditions on position and velocity near impact in tennis[END_REF], three frames around the ball impact (determined according to [START_REF] Creveaux | Joint Kinetics to Assess the Influence of the Racket on a Tennis Player's Shoulder[END_REF] were deleted; then the data were filtered separately before and after the ball impact.

Glenohumeral contact forces

The joint kinematics and scaled models were used as input of the static optimisation procedure [START_REF] Delp | OpenSim: open-source software to create and analyze dynamic simulations of movement[END_REF] in order to obtain muscle activations required to perform the forehand drives. Briefly, at each sample time (𝑡), the objective function (𝐽) to minimise consisted in the quadratic sum of muscle activations (𝑎) and the quadratic sum of residual torques (i.e. artificial joint actuators used to solve the numerical problem when muscles cannot reproduce the joint torque computed with inverse dynamics procedure) (𝜏 𝑟𝑒𝑠 ) at each degree of freedom (𝑛), subject to two constraints 1) the joint torques calculated from muscle activations were equal to the torques (𝜏) computed from the inverse dynamic procedure (Eq. 2) and 2) the glenohumeral forces were inside a friction polygon ensuring the stability of the glenohumeral joint (Eq. 3) [START_REF] Dickerson | A mathematical musculoskeletal shoulder model for proactive ergonomic analysis[END_REF]. The glenohumeral contact forces between the humeral head and scapula 𝑅 ⃗ 𝐺𝐻 were calculated using the jointReaction algorithm of OpenSim 3.2 [START_REF] Delp | OpenSim: open-source software to create and analyze dynamic simulations of movement[END_REF][START_REF] Steele | Compressive tibiofemoral force during crouch gait[END_REF]):

subject to min 𝑎(𝑡) 𝑚 𝐽(𝑡) = 𝑐 1 * ∑ (𝑎(𝑡) 𝑚 ) 2 139 𝑚=1 + 𝑐 2 * ∑(𝜏 𝑟𝑒𝑠 (𝑡) 𝑛 ) 2 , 18 𝑛=1 (Eq. 1) ∑ 𝑟 𝑚,𝑗 • [𝑎(𝑡) 𝑚 • 𝑓(𝐹 𝑚 0 ,
[𝑀] ℎ𝑢𝑚𝑒𝑟𝑢𝑠 is the matrix of inertial properties of the humerus, 𝑎 ℎ𝑢𝑚𝑒𝑟𝑢𝑠 denotes the six dimensional angular and linear accelerations of the humerus, 𝑅 ⃗ 𝑒𝑙𝑏𝑜𝑤 is the force and moment of the ulna on the humerus; 𝐹 𝑚𝑢𝑠𝑐𝑙𝑒𝑠 and 𝐹 𝑔𝑟𝑎𝑣𝑖𝑡𝑦 are the muscle and gravitational forces and moments acting on the humerus. Glenohumeral contact forces were initially calculated in the scapula reference system. In order to express these forces in the glenoid reference system, three landmarks were located on the scapula of the generic Opensim model (most anterior, posterior and inferior points of the edge of the glenoid). These landmarks were used to define

[ 𝛼 1 𝜇 1 -1 0 𝛼 2 𝜇 2 -1 -1 𝛼 3 𝜇 3 0 -1 𝛼 4 𝜇 4 1 -1 𝛼 5 𝜇 5 1 0 𝛼 6 𝜇 6 1 1 𝛼 7 𝜇 7 0 1 𝛼 8 𝜇 8 -1 1] . [ 𝑅 𝐺𝐻 𝑛 𝑅 𝐺𝐻 𝑠1 𝑅 𝐺𝐻 𝑠2
] ≥ 𝟎 , (Eq. 3)

𝑅 ⃗ 𝐺𝐻 = [𝑀] ℎ𝑢𝑚𝑒𝑟𝑢𝑠 • 𝑎 ℎ𝑢𝑚𝑒𝑟𝑢𝑠 -(𝑅 ⃗ 𝑒𝑙𝑏𝑜𝑤 + ∑ 𝐹 𝑚𝑢𝑠𝑐𝑙𝑒𝑠 + 𝐹 𝑔𝑟𝑎𝑣𝑖𝑡𝑦 ), (Eq. 4)

the reference system of the glenoid. Finally, the transformation matrix scapula-to-glenoid was used to compute glenohumeral contact forces in the glenoid reference system.

Analysis

Among all forehand drives performed, only the three for which the ball bounced in the opposite court and with similar ball post-impact velocities were taken into consideration in the subsequent analysis. Four key-events were detected, such as the beginning of the shoulder turn, first forward movement of the racket, ball impact, and highest elbow height after impact [START_REF] Ryu | An electromyographic analysis of shoulder function in tennis players[END_REF], in order to define three successive phases: (1) the backswing;

(2) the forward swing and (3) the follow-through.

For each phase, the mean and maximal values of the compressive, shearing and total glenohumeral contact forces were calculated. In line with a previous study [START_REF] Charbonnier | Shoulder motion during tennis serve: dynamic and radiological evaluation based on motion capture and magnetic resonance imaging[END_REF], the direction of the glenohumeral contact forces was expressed by dividing the glenoid into eight sections (Figure 2). Then, the percentage of glenohumeral contact forces inside each of the eight sections was computed. Finally, for each variable cited above, the values obtained either for the flat or topspin forehand drives were averaged separately, in order to obtain one value per variable and per forehand drive technique.

In order to evaluate the model outputs, mean and maximal residual torques were computed and compared to the joint torques calculated by the inverse dynamic procedure. In addition, the mean activation of nine muscles (anterior, middle, posterior deltoids; pectoralis major; latissimus dorsi; serratus anterior; infraspinatus; supraspinatus and subscapularis) was calculated and ranked by order of intensity to be compared with EMG data from the literature.

The rank comparison was chosen instead of the comparison of activation values since musculoskeletal model activations are different from experimental normalised EMG.

Results

Evaluation of the model outputs

Regardless the forehand drive technique, the maximal residual torques were on average 14.7 ± 2.3, 8.4 ± 4.9 and 22.6 ± 7.2 times smaller than the corresponding maximal joint torques for the sterno-clavicular, acromio-clavicular and glenohumeral joint respectively. Greater differences were observed concerning the mean residual torques which were in average 29.7 ± 7.1, 14.3 ± 6.8 and 37.6 ± 10.5 times smaller than the corresponding mean joint torques for the sterno-clavicular, acromio-clavicular and glenohumeral joint, respectively.

The qualitative analysis of the muscle activations enabled to point out low activations for all muscles during the backswing phase (Figure 3). The pectoralis major/minor, anterior deltoid, subscapularis and upper trapezius were highly activated in comparison to the other shoulder muscles during the forward swing phase (Figure 3). Finally, the middle and posterior deltoids, latissimus dorsi, infraspinatus, upper and middle trapezius were mainly involved during the follow-through phase. The ranking order of muscle mean activation between phases was overall similar to those reported by [START_REF] Ryu | An electromyographic analysis of shoulder function in tennis players[END_REF] (Table 1).

Forehand drive analysis

The mean ball velocities were 31.5 ± 5.5 m/s for flat and 27.4 ± 4.6 m/s for the topspin forehand drives. The norms of the 3D racket velocity one frame before the impact were on average 20.2 ± 4.5 m/s for flat and 21.7 ± 5.3 m/s for the topspin forehand drives. Finally, the mean racket vertical velocities were 6.6 ± 2.1 m/s for flat and 11.1 ± 1.9 m/s for the topspin forehand drives.

The linear mixed models revealed only a main effect of the phase on the mean and maximal compressive, shearing and total glenohumeral contact forces (χ²(2)ϵ[68.7, 87], p< 0.001). The glenohumeral contact forces during the forward swing phase were in average 1.25 time greater than during the follow-through phase, and 5.8 times greater than during the backswing phase (Table 2 andfigure 4).

Concerning the repartition of the glenohumeral contact forces in the eight glenoid sections, the chi-square test of independence revealed no dependency between the forehand drive technique and the glenoid sections either for the backswing (χ²(7)=0.34, p=0.99), forward swing (χ²(7)=2.41, p=0.93) or follow-through phases (χ²(7)=8.59, p=0.28). Regardless the forehand drive technique, the chi-square test for homogeneity revealed for each phase that the distribution of the glenohumeral contact forces in the sections of the glenoid was not homogeneous (χ²(7)=462, p<0.001; χ²(7)=440, p<0.001; χ²(7)=167, p<0.001, respectively for the backswing, forward swing and follow-through phases). For the backswing and forward swing phases, the greatest residual of the chi-square tests was observed for the "anteriorSuperior" section (Figure 2), while concerning the follow-through phase, the greatest residual of the chi-square tests was observed for the "superiorAnterior" section (see Table T1 of the residuals in the supplementary file).

Discussion and implications

This study aimed to investigate the contact forces at the glenohumeral joint during the flat and topspin forehand drives in advanced tennis players. The first findings were that the forehand drive technique, i.e. flat or topspin, did not change the glenohumeral contact forces undergone by the tennis player. The second findings were that the maximal contact force undergone by the glenohumeral joint occurred during the forward swing phase, and pointed toward the anterior-superior part of the glenoid.

Evaluation of the model outputs

As the computed glenohumeral contact forces resulted from the modelled muscle forces, the validity of our model needed to be evaluated. The values for the maximal and mean residual torques involved during the forehand drive motion were between 8.4 and 37.6 times smaller than the maximal and mean torques computed with the inverse dynamic procedure. These results meant that the muscles included in the model were sufficient to ensure the joint torques necessary to perform the forehand drives [START_REF] Hicks | Is my model good enough? Best practices for verification and validation of musculoskeletal models and simulations of movement[END_REF].

Regardless the forehand drive technique, the orders of the magnitude of muscle activations between phases was similar than the normalised EMG data of [START_REF] Ryu | An electromyographic analysis of shoulder function in tennis players[END_REF]. Only three muscles had a different ranking, namely the infraspinatus, supraspinatus and middle deltoid muscles (Table 1). The mean normalised EMG levels of these muscles however present small differences between the phases of the forehand drive, i.e. 3 to 11% [START_REF] Ryu | An electromyographic analysis of shoulder function in tennis players[END_REF], potentially explaining the discrepancies in the rank between studies. The changes in racket specifications over the last 30 years may also result in differences in player's motion, and then in muscle demand, hence explaining some of the discrepancies between the two studies. In comparison with [START_REF] Genevois | Trunk and Shoulder Muscle Coordination during One, Two-Handed Medicine-Ball Side Throws and Tennis Forehand Drive[END_REF] and [START_REF] Rota | Influence of fatigue on upper limb muscle activity and performance in tennis[END_REF], we also observed that the mean activations of the anterior deltoid and pectoralis major were greater than the mean activations of the latissimus dorsi and middle deltoid (Figure 3).

In summary, our model seemed to respect the salient characteristic of the forehand drive performed by the players. Although our computed glenohumeral contact forces could not be compared with in-vivo data (see limitations section), we assume that they were suitable for further interpretation.

Glenohumeral contact forces

The contribution of the shoulder complex to the racket velocity production remains similar whatever the technique required to hit a forehand drive [START_REF] Takahashi | The role of upper limb segment rotations in the development of spin in the tennis forehand[END_REF]. This outcome may partly explain the lack of differences in the glenohumeral contact forces computed during both the flat and topspin forehand drives. It is also possible that our model was not sufficiently accurate to detect the small changes in glenohumeral contact forces with respect to the forehand drive technique. Grouping the results for both techniques of shots nevertheless provided new information on the glenohumeral contact forces during the tennis forehand drive.

The achievement of a forehand drive requires firstly a slow motion, then a rapid acceleration, and finally a deceleration of the upper limbracket complex [START_REF] Elliott | A biomechanical comparison of the topspin and backspin forehand approach shots in tennis[END_REF]. Such a motion pattern may explain the differences observed in maximal glenohumeral contact forces between the three phases, e.g. 559 ± 145 N, 3573 ± 1383 N and 2327 ± 1162 N, for the backswing, forward swing and follow-through phase respectively. These results suggested that the player's shoulder was not at the same level of risk for injury throughout the forehand drive motion. During the backswing phase, a trunk rotation occurs to place it perpendicularly to the net [START_REF] Elliott | A biomechanical comparison of the topspin and backspin forehand approach shots in tennis[END_REF], while the humerus abducts, extends, and externally rotates to take back the racket. The activation of the teres minor muscle may contribute to place the humerus in the adequate position at the end of the backswing, whereas the pectoralis minor muscle mainly acts to anteriorly tilt the scapula (Rogowski, Creveaux, Cheze, & Dumas, 2014) (Figure 3). The anterior and superior orientation of the glenohumeral contact forces may be partly related to the early activation of the anterior deltoid muscle, which is involved in the stretch-shorten cycle movement to contribute to a powerful shot [START_REF] Wilson | The effect on performance of imposing a delay during a stretch-shorten cycle movement[END_REF]. As the positioning of the racket at the end of the backswing phase requires low muscle activations, the shearing forces and consequently the compressive forces (that ensure the glenohumeral stability) remained at low levels. During the forward swing phase, a large demand is placed on the pectoralis major/minor, anterior deltoid and subscapularis muscles to achieve a rapid humeral horizontal adduction and internal rotation (Figure 3) [START_REF] Ryu | An electromyographic analysis of shoulder function in tennis players[END_REF]. As these muscles cross the glenohumeral joint, their increased activation automatically led to raise the compressive and shearing glenohumeral contact forces and to orientate them toward the anterior section of the glenoid. It may be hypothesised that the activation of the latissimus dorsi, teres minor, infraspinatus, and rhomboid became crucial to counteract the increased shearing glenohumeral force. Their activation may have contributed to the increased compressive glenohumeral force, ensuring then the glenohumeral stability [START_REF] Dickerson | A mathematical musculoskeletal shoulder model for proactive ergonomic analysis[END_REF][START_REF] Lippitt | Mechanisms of glenohumeral joint stability[END_REF]. During the follow-through phase, the glenohumeral contact forces decreased, even if they remained relatively high in comparison to the backswing phase.

This may be explained by the high velocity of the arm during the follow-through phase [START_REF] Marshall | Long-axis rotation: the missing link in proximal-todistal segmental sequencing[END_REF]. The middle deltoid and upper trapezius were involved in the humeral abduction, and may contribute to upwardly orientate the glenohumeral contact forces.

The middle trapezius, infraspinatus, teres minor and posterior deltoid muscles then may contract eccentrically to resist to the anterior glenohumeral shearing forces. Although our model did not allow translations of the humeral head, the observation of the orientation of the glenohumeral contact forces leads to the same conclusions than [START_REF] Ladermann | Kinematics of the shoulder joint in tennis players[END_REF]. The muscle forces produced during the forehand drive result in glenohumeral contact forces pointing in a forward and upward direction; the consequence may be a translation of the humeral head that may cause an anterior-superior humero-glenoid impingement.

Limitations

The first limitation of this study was that the glenohumeral contact forces were estimated and not measured in-vivo. Nevertheless, only invasive methods make possible to measure glenohumeral contact forces. To the best of our knowledge, few studies measured in-vivo glenohumeral contact forces, only focusing on arm elevation, isometric forces [START_REF] Nikooyan | Validation of the Delft Shoulder and Elbow Model using in-vivo glenohumeral joint contact forces[END_REF] and daily living activities [START_REF] Westerhoff | In vivo measurement of shoulder joint loads during activities of daily living[END_REF][START_REF] Westerhoff | In vivo measurement of shoulder joint loads during walking with crutches[END_REF], but not during sport movements. In addition, to our knowledge, glenohumeral contact forces estimated through musculoskeletal model were only investigated during wheelchair tasks [START_REF] Holloway | Linking wheelchair kinetics to glenohumeral joint demand during everyday accessibility activities[END_REF][START_REF] Van Der Helm | Quasi-static analysis of muscle forces in the shoulder mechanism during wheelchair propulsion[END_REF][START_REF] Van Drongelen | Load on the shoulder complex during wheelchair propulsion and weight relief lifting[END_REF], but not for sport movements.

Although the comparison between our results and the previous studies is not obvious, our computed contact forces (Table 2) were up to four times greater than the maximal glenohumeral forces measured in-vivo with an instrumented prosthesis during arm elevation (≈800 N.) [START_REF] Nikooyan | Validation of the Delft Shoulder and Elbow Model using in-vivo glenohumeral joint contact forces[END_REF]. In comparison to other musculoskeletal models, we found glenohumeral contact forces in the same range than those estimated during wheelchair propulsion [START_REF] Holloway | Linking wheelchair kinetics to glenohumeral joint demand during everyday accessibility activities[END_REF][START_REF] Van Der Helm | Quasi-static analysis of muscle forces in the shoulder mechanism during wheelchair propulsion[END_REF] or during vertical weight relief lift from a wheelchair [START_REF] Van Drongelen | Load on the shoulder complex during wheelchair propulsion and weight relief lifting[END_REF]. Consequently, the values of the glenohumeral contact forces obtained in this study must be taken with caution even if they do not seem to be abnormal in comparison to the literature.

The second limitation was that our model enabled only three rotations at the glenohumeral joint and no translation. Although the computing of the glenohumeral contact forces is probably affected by the number of degrees of freedom, the orientation of the glenohumeral contact forces calculated in our study led to similar conclusions than those of

  significant difference between the backswing and forward swing phases (* for p<0.05; ** for p<0.01; *** for p<0.001); ǂ indicates a significant difference between the forward swing and follow-through phases ( ǂ for p<0.05; ǂ ǂ for p<0.01; ǂ ǂ ǂ for p<0.001); ۲ indicates a significant difference between the backswing and follow-through phases (۲ for p<0.05; ۲۲ for p<0.01; ۲۲۲ for p<0.001).

Figure 2 .Figure 3 .

 23 Figure 2. The glenoid was divided into eight sectors based on Charbonnier et al. (2015) in

Figure 4 .

 4 Figure 4. Compressive (dashed line), shearing (solid line) and total (dotted line)

Figure 5 .

 5 Figure 5. Mean ± standard deviation distribution (%) of the glenohumeral contact forces

  𝑙 𝑚 , 𝑣 𝑚 )] 𝑙 𝑚 is the muscle model length; 𝑣 𝑚 denotes the muscle model shortening/lengthening velocity; 𝑓(𝐹 𝑚 0 , 𝑙 𝑚 , 𝑣 𝑚 ) is its force-length-velocity surface relationship; 𝑟 𝑚,𝑗 is the moment arm about j th joint axis; 𝑐 1 and 𝑐 2 referring to weighting

	with m referring to the 139 muscle-tendon-units; 𝐹 𝑚 0 is the maximum isometric force of the
	modelled muscles m; factors; 𝑅 𝐺𝐻 𝑛 , 𝑅 𝐺𝐻 𝑠1 , 𝑅 𝐺𝐻
	139	18
		+ ∑ 𝜏 𝑟𝑒𝑠 (𝑡) 𝑛	= 𝜏(𝑡) 𝑗 ,	(Eq. 2)
	𝑚=1	𝑛=1

𝑠2

: the normal, posterior-anterior and superior-inferior glenohumeral contact force components; 𝜇 𝑖 : the dislocation thresholds equal to [0.29, 0.33, 0.51, 0.35, 0.30, 0.43, 0.56, 0.4]

[START_REF] Dickerson | A mathematical musculoskeletal shoulder model for proactive ergonomic analysis[END_REF]

for each polygon vertex (i), 𝛼 𝑖 : optimised coefficients (Wieber, 2001) to best match with

Dickerson's polygon (2007)

.

Table 1 .

 1 [START_REF] Ladermann | Kinematics of the shoulder joint in tennis players[END_REF] who had implemented glenohumeral translation in their kinematic model. In addition, our kinematical model obtained only from skin markers did not enable to estimate accurately the very small glenohumeral translations occurring during forehand drives (less than 2.8 mm for forehand drive mimic)[START_REF] Dal Maso | Glenohumeral translations during range-of-motion movements, activities of daily living, and sports activities in healthy participants[END_REF]. The third limitation of our study was that the muscle forces of the model were not specific to those of the participants. It may be possible that the tennis players of this study had different maximal isometric muscle forces than those implemented in the generic Delft Shoulder and Elbow model. Further studies are needed with participant-specific musculoskeletal model to estimate more precisely glenohumeral contact forces. Regardless the forehand drive technique (flat or topspin), the tennis players underwent the greatest glenohumeral contact forces during the forward swing, then during the follow-through and finally during the backswing phase. Most of the glenohumeral contact forces pointed toward the anterior-superior part of the glenoid. This study brings new knowledge on the glenohumeral loadings during real sport motion, and provides information that may help the sport clinicians and tennis coaches on the causative factors for shoulder problems. Ranked order between phases by intensity of muscle activations or normalised EMG for seven shoulder muscles in comparison to the data of[START_REF] Ryu | An electromyographic analysis of shoulder function in tennis players[END_REF]. The greater the rank, the greater the activation intensity or normalised EMG.

	Conclusion
	This study was the first to estimate glenohumeral contact forces during forehand drives,
	through musculoskeletal modelling.

difference in rank order between our model and Ryu's data.Table 2 .

 2 Mean ± standard deviation of the mean and maximal compressive, shearing and total glenohumeral forces with respect to the phase (backswing, forward swing and followthrough). As no effect of the forehand drive technique has been observed, values for the flat and topspin forehand drives were averaged.

		Backswing	Forward swing	Follow-through	p-values
	Maximal
	Compressive (N)	530 ± 137	3396 ± 1323	2210 ± 1103	***, ǂ ǂ ǂ,۲۲۲
	Shear (N)	176 ± 49	1116 ± 410	754 ± 361	***, ǂ ǂ ǂ, ۲۲۲
	Total (N)	559 ± 145	3573 ± 1383	2327 ± 1162	***, ǂ ǂ ǂ, ۲ ۲۲
	Mean
	Compressive (N)	262 ± 65	1513 ± 643	1215 ± 596	***, ǂ,۲۲۲
	Shear (N)	87 ± 23	498 ± 211	394 ± 221

***, ǂ,۲۲۲

Statistical analysis

The interaction effect between the forehand drive technique (flat vs. topspin; fixed effect) and the phase (backswing vs. forward swing vs. follow-through; fixed effect) on the mean and maximal compressive, shearing and total glenohumeral contact forces was tested using linear mixed models. Linear mixed-model is an alternative method to the ANOVA on repeated measures that may be more advantageous especially with categorical data [START_REF] Barr | Random effects structure for confirmatory hypothesis testing: Keep it maximal[END_REF]. As within-participants repeated measures were performed, participants were entered as random intercept. To avoid the effect of a different racket velocity at the frame before the impact between the flat and topspin forehand drives, the racket velocity was also entered as random intercept. Finally, as the forehand drive technique might have different effect with respect to the participants and/or the racket velocity, forehand drive technique was also entered as random slope [START_REF] Barr | Random effects structure for confirmatory hypothesis testing: Keep it maximal[END_REF]. The p-values were obtained by likelihood ratio tests of the full model against the model without the effect in question. The level of significance was set at p<0.008 (Bonferroni correction 0.05/6 variables). When a main effect was revealed by the linear mixed-model, post-hoc pairwise comparisons were performed using the Tukey's honestly significant difference procedure with a significant p-value set at 0.05. The linearity, homoscedasticity and normality of the linearmixed model residuals were graphically controlled. All models were performed using the package lme4 of R software (R 3.2, RCore Team 2014, Vienna, Austria).

The chi-square test of independence was used to assess if the proportion of glenohumeral contact forces inside the eight glenoid sections was dependent of the forehand drive technique. Finally, the difference in the proportion of glenohumeral contact forces between each glenoid section was tested using the chi-square test for homogeneity of proportion. All chi-square tests were executed using R software.


Scapular kinematics during scaption in competitive swimmers

Keywords: Skill-level, Swimming, Shoulder complex adaptations, Scapular Dyskinesis, Shoulder

This study aimed 1) to describe and compare scapular kinematics between three groups of swimmers of different levels and a group of non-swimmers, and 2) to assess whether swimming practice alters the asymmetries in scapular kinematics between the dominant and non-dominant sides, both during unilateral arm raising and lowering in the scapular plane. Scapular kinematics rotation. In conclusion, the findings of the study pointed out that swimming practice generated protracted shoulders and removed bilateral differences in scapular upward rotation during scaption, while accumulation of swimming practice at elite level enlarged scapular internal rotation.

were assessed bilaterally during arm raising and lowering in the scapular plane using an electromagnetic system in 42 healthy males, which were split into four groups: control (n=11), adolescent elite swimmers (n=11), adult elite swimmers (n=10), and club-level adult swimmers (n=10). One-Way ANOVA SPM(t) on two repeated measures showed that the three groups of swimmers had more protracted shoulder between 30° and 90° of arm raising and lowering (p<0.001). The three groups of swimmers presented no bilateral difference in scapular upward rotation, while the dominant scapula was more upwardly rotated than the non-dominant one between 74° and 104° of arm elevation in the control group (p<0.001). The scapula of adult elite swimmers was more internally rotated between 67° and 116° of humeral elevation during arm raising, and between 81° and 54° during arm lowering in comparison to the other swimming and control groups (p≤0.02), who presented similar scapular positioning in internal

Introduction

Swimming at competitive level demands a training volume ranged between 9 km/week for club-level swimmers and 110 km/week or more for international level swimmers [START_REF] Sein | Shoulder pain in elite swimmers: primarily due to swim-volume-induced supraspinatus tendinopathy[END_REF]. The corresponding number of arm revolutions is estimated between 3000 and 44 000 per week [START_REF] Bradley | Review of shoulder injuries and shoulder problems in competitive swimmers[END_REF]) which cumulate during the 40 weeks [START_REF] Hibberd | Effect of a 6-week strengthening program on shoulder and scapular-stabilizer strength and scapular kinematics in division I collegiate swimmers[END_REF] of each swimmer's career season. Repeated arm revolutions involve a large amount of musculoskeletal loads onto the shoulder complex, which is known to generate alteration in shoulder kinematics [START_REF] Hibberd | Effect of a 6-week strengthening program on shoulder and scapular-stabilizer strength and scapular kinematics in division I collegiate swimmers[END_REF][START_REF] Hibberd | Comparison of Upper Extremity Physical Characteristics Between Adolescent Competitive Swimmers and Nonoverhead Athletes[END_REF], although these alterations in relation with skill-level of the swimmers are not yet well described.

During free-style stroke, both arms act alternatively but in the same fashion [START_REF] Bak | Shoulder strength and range of motion in symptomatic and pain-free elite swimmers[END_REF]. Depending on the studies [START_REF] Pink | The normal shoulder during freestyle swimming. An electromyographic and cinematographic analysis of twelve muscles[END_REF][START_REF] Chollet | A new index of coordination for the crawl: description and usefulness[END_REF][START_REF] Yanai | Shoulder impingement in front-crawl swimming: II. Analysis of stroking technique[END_REF], each arm revolution may be divided into three successive phases.

The catch phase occurs from the hand entry in the water, during which the shoulder is elevated to reach forward maximally [START_REF] Yanai | Shoulder impingement in front-crawl swimming: II. Analysis of stroking technique[END_REF]. Then the pull phase demands powerful humeral adduction, internal rotation and extension (Pink, Perry et al. 1991, Du and[START_REF] Du | Three dimensional motion of shoulder complex during front crawl swimming[END_REF].

Finally, the recovery phase is achieved by a humeral abduction and external rotation to place the hand forward for the following arm entry [START_REF] Yanai | Shoulder impingement in front-crawl swimming: II. Analysis of stroking technique[END_REF]. In consequence, the bilateral nature of swimming may involve similar adaptations in the dominant and nondominant shoulders, [START_REF] Madsen | Training induces scapular dyskinesis in pain-free competitive swimmers: a reliability and observational study[END_REF], leading to annihilate the bilateral shoulder asymmetry observed in sedentary population [START_REF] Matsuki | In vivo 3-dimensional analysis of scapular kinematics: comparison of dominant and nondominant shoulders[END_REF][START_REF] Morais | Scapular positioning assessment: Is side-to-side comparison clinically acceptable?[END_REF].

Acute response to excessive repeated arm revolutions involves an alteration in scapular kinematics in swimmers. [START_REF] Madsen | Training induces scapular dyskinesis in pain-free competitive swimmers: a reliability and observational study[END_REF] observed that 82% of their adolescent swimmers presented scapular dyskinesia during arm elevation in the scapular plane after 25 minutes of swimming training. Prevalence of such scapular dyskinesia increased through a training session [START_REF] Madsen | Training induces scapular dyskinesis in pain-free competitive swimmers: a reliability and observational study[END_REF]. Alterations in scapular kinematics, such as increased internal rotation, protraction and elevation has been also observed after a 6-week swimming training period in young adults [START_REF] Hibberd | Effect of a 6-week strengthening program on shoulder and scapular-stabilizer strength and scapular kinematics in division I collegiate swimmers[END_REF]. Besides, long-term swimming is known to enlarge and tighten the anterior shoulder musculature causing postural adaptations, such as forward head and rounded shoulders in adolescents [START_REF] Laudner | Forward Shoulder Posture in Collegiate Swimmers: A Comparative Analysis of Muscle-Energy Techniques[END_REF][START_REF] Hibberd | Comparison of Upper Extremity Physical Characteristics Between Adolescent Competitive Swimmers and Nonoverhead Athletes[END_REF]. However, all these studies have been performed on adolescents and young adults (between 16.5 and 19 years old on average), while the amount of shoulder adaptations due to repeated arm revolutions may depend on the mileage per week, the number of years of practice (partially related to the age of the swimmer) and the level of practice [START_REF] Gordon | A shorter guide to long term athlete development (LTAD)[END_REF]).

Finally, shoulder postural adaptations observed in swimmers may affect the scapular positioning during arm motion. Indeed, previous study involving a healthy adult population has shown that increased forward posture, demands more shoulder elevation, less upward rotation, less posterior tilt and more internal rotation to elevate the arm in the scapular plane [START_REF] Kebaetse | Thoracic position effect on shoulder range of motion, strength, and three-dimensional scapular kinematics[END_REF]). As such scapular positioning has been associated with various shoulder injuries [START_REF] Kibler | Clinical implications of scapular dyskinesis in shoulder injury: the 2013 consensus statement from the 'Scapular Summit[END_REF], it is important to define the normal scapular kinematics in healthy swimmer athletes in order to contribute to shoulder injury prevention.

The objectives of this study were 1) to describe and compare scapular kinematics between three groups of swimmers of different levels and a group of non-swimmers, and 2) to assess whether swimming practice alters the asymmetries in scapular kinematics between the dominant and non-dominant sides, both during unilateral arm raising and lowering in the scapular plane. It was hypothesized that the swimmers' shoulder adapts to the swimming practice by increasing shoulder elevation and protraction as well as by increasing scapular internal rotation and anterior tilt while decreasing scapular upward rotation and eliminating handedness effect.

Methods

Participants

Forty-two healthy male adults participated to this study. They signed an informed consent document, which was approved by the Ethical Committee "Sud-Est II" (IRB 00009118). None of the participants declared any shoulder and upper limb symptoms and injuries during the 12 months prior to the experimentation. Then, the participants were split into four groups (Table 1). The first group (G0_Cont) was composed of 11 males that did not practice swimming or any sports involving the shoulder and upper limbs, and was used as the control group. The second group (G1_AdoElit) included 11 adolescent elite swimmers. The third group (G2_AduElit) included 10 adult elite swimmers. The last group (G3_AduClub) was composed of 10 club-level adult swimmers. The practice level was determined by the French federation quotation, which attributes between 1 and 1500 points to the swimmer based on his/her best race during the year preceding the study (French Federation of Natation, 2016, https://ffn.extranat.fr/html/ressources/nat/table_cotation_2017.pdf).

Instrumentation and data collection

To perform the kinematic analysis, an electromagnetic device, which has already been tested to assess shoulder kinematics [START_REF] El Habachi | A parallel mechanism of the shoulder-application to multi-body optimisation[END_REF][START_REF] Gillet | Scapulothoracic kinematics during scaption after one year of tennis practice in elite girl players[END_REF][START_REF] Seitz | A Comparison of Change in 3d Scapular Kinematics with Maximal Contractions and Force Production with Scapular Muscle Tests between Asymptomatic Overhead Athletes with and without Scapular Dyskinesis[END_REF], was used (100Hz; Trackstar, Ascension Technology Corporation, Chicago, Ill). It was composed of five sensors located on incisura jugularis, flat portion of the right and left acromion angles, and distal portion of the right and left humerus.

In order to calibrate the kinematic model and define segments reference system, a sixth sensor was taped to a stylus used to digitalize bony landmarks (T8, processus xiphoideus, C7, incisura jugularis, and for both sides, scapular angulus acromialis, trigonum scapulae, angulus inferior, humeral medial and lateral epicondyle).

In a previous experiment (non-published data), we observed that our electromagnetic device used in the same conditions than the present study ensured fair to good intersession relative reliability (ICC[2,1]=0.81±0.15) and an absolute reliability (SEM) of 4.2±1.4°. In addition, a previous study reported errors of scapular kinematics during arm elevation included between 5 and 9° in comparison to the palpation method [START_REF] El Habachi | A parallel mechanism of the shoulder-application to multi-body optimisation[END_REF].

Procedure

Prior to the tests, the participants kept a standing upright posture for further calibration. Then they performed four arm circumductions to determine joint center of rotation. Finally, they performed several arms elevation with a maximal amplitude to be familiarized with the procedure and the instruments. The tests consisted in raising and lowering the arm in the scapular plane with the thumb pointed in the upward direction. The participants had to keep the elbow straight throughout the movement. Two cycles of unilateral arm raising/lowering were performed with the dominant (i.e. writing hand) and non-dominant arms in a controlled random order. In order to ensure that the movements were performed in the scapular plane, a goniometer was used to set the plane of elevation (30° anterior to the frontal plane). Thereafter, a vertical pole was located in scapular plane of elevation and guided the participant throughout the movement. Finally, a cycle duration lasted four seconds (two seconds for raising and lowering) [START_REF] Ludewig | Alterations in shoulder kinematics and associated muscle activity in people with symptoms of shoulder impingement[END_REF].

Kinematics

Raw data were filtered using a low-pass 4 th order Butterworth filter with a cut-off frequency of 10 Hz. The local coordinate systems were defined in line with the recommendations of the International Society of Biomechanics [START_REF] Wu | ISB recommendation on definitions of joint coordinate systems of various joints for the reporting of human joint motion--Part II: shoulder, elbow, wrist and hand[END_REF]. Firstly, clavicular orientation relative to the thorax were described by two rotations, namely protraction/retraction and elevation/depression [START_REF] Mcclure | Direct 3-dimensional measurement of scapular kinematics during dynamic movements in vivo[END_REF][START_REF] Myers | Scapular position and orientation in throwing athletes[END_REF] (Figure1). To that aim, the vector from the incisura jugularis (IJ) and Acromion Angle (AA) points was used. Clavicular elevation/depression corresponded the angle between the vector 𝐼𝐽 -𝐴𝐴 ⃗⃗⃗⃗⃗⃗⃗⃗⃗⃗⃗⃗⃗⃗⃗ and the transversal plane of the thoracs that bisects IJ point. For the clavicular protraction/retraction, the vector 𝐼𝐽 -𝐴𝐴 ⃗⃗⃗⃗⃗⃗⃗⃗⃗⃗⃗⃗⃗⃗⃗ was projected onto the transverse plane bisecting IJ.

Then, clavicular protraction/retraction was the angle between the projected vector and the frontal plane of the thorax that bisects IJ [START_REF] Mcclure | Direct 3-dimensional measurement of scapular kinematics during dynamic movements in vivo[END_REF][START_REF] Myers | Scapular position and orientation in throwing athletes[END_REF]. Secondly, scapular orientation with respect to the thorax were computed with Euler angle decompositions (Figure 1). Scapulothoracic rotations were defined as internal/external rotation, upward/downward rotation, and anterior/posterior tilt, using YXZ rotation sequence.

Humerothoracic rotations were determined as the plane of elevation, elevation, and rotation using YXY rotation sequence. In order to ensure a sufficient accuracy of the assessment of scapular kinematics, arm elevations were analyzed between 30 and 120° of humerothoracic elevation (Karduna, McClure et al. 2001, Senk and[START_REF] Senk | A new method for motion capture of the scapula using an optoelectronic tracking device: a feasibility study[END_REF]. The mean of the two trials were computed for the analysis.

Results

In all groups, the shoulder elevated during arm raising and depressed during arm lowering (see supplementary file S1). Statistical analysis revealed no significant effect of interaction, or group or laterality for shoulder elevation/depression either during arm raising or lowering.

The shoulder retracted during arm raising and protracted during arm lowering (Figure 2 and supplementary file S2). ANOVA revealed only a significant effect of the group for the shoulder protraction/retraction between 30 and 120° of humeral elevation during the arm raising and lowering. Post-hoc tests showed that the shoulders were more retracted in G0_Cont in comparison to G1_AdoElit, G2_AduElit and G3_AduClub (p<0.001, p=0.03 and p<0.001, respectively). Shoulders were more retracted for G2_AduElit when compared to G1_AdoElit and G3_AduClub (p=0.004, p=0.04, respectively), while similar shoulder retraction was observed for the shoulders of G1_AdoElit and G3_AduClub.

For all groups, the scapula internally rotated during arm raising and externally rotated during arm lowering (Supplementary file S3). ANOVA revealed only a significant effect of the group between 67° and 116° of humeral elevation during arm raising, and between 81° and 54° during arm lowering (Figure 3). The scapular positioning in internal rotation was similar in G0_Cont, G1_AdoElit and G3_AduClub, while G2_AduElit presented increased scapular internal rotation (p=0.005, p=0.02 and p=0.007, respectively).

In all groups, the scapula upwardly rotated during arm raising and downwardly rotated during arm lowering (Figure 4). ANOVA revealed a significant effect of the interaction group*laterality between 74° and 104° of humeral elevation during arm raising. Post hoc tests showed a significant side-to-side difference in G0_Cont (p<0.001), while no significant sideto-side difference was observed in all the other groups of swimmers. The non-dominant scapular upward rotation was significantly higher in G0_Cont when compared to G2_AduElit (p=0.03) and G3_AduClub (p=0.01), while no difference was observed between the four groups for the dominant side.

In all groups, the scapula posteriorly tilted during arm raising and anteriorly tilted during arm lowering (supplementary file S4). Statistical analysis revealed no significant effect of interaction, or group or laterality for scapular anterior/posterior tilt either during arm raising or lowering. # means a significant difference between G0_Cont and G1_AdoElit at p<0.05 inside the grey shaded zone † means a significant difference between G0_Cont and G2_AduElit at p<0.05 inside the grey shaded zone * means a significant difference between G0_Cont and G3_AduClub at p<0.05 inside the grey shaded zone § means a significant difference between G2_AduElit and G3_AduClub at p<0.05 inside the grey shaded zone ‡ means a significant difference between G2_AduElit and G1_AduClub at p<0.05 inside the grey shaded zone † means a significant difference between G0_Cont and G2_AduElit at p<0.05 inside the grey shaded zone ‡ means a significant difference between G2_AduElit and G1_AduClub at p<0.05 inside the grey shaded zone § means a significant difference between G2_AduElit and G3_AduClub at p<0.05 inside the grey shaded zone

Discussion

The aim of this study was 1) to describe and compare scapular kinematics between three groups of swimmers of different levels and a group of non-swimmers, and 2) to assess whether swimming practice alters the asymmetries in scapular kinematics between the dominant and non-dominant sides, both during unilateral arm raising and lowering in the scapular plane. The main findings confirmed that swimming practice generated an increased clavicular protraction and removed bilateral differences in scapular upward rotation during scaption. The findings of this study also suggested that alterations in scapular internal rotation positioning were related to the swimming practice level.

The achievement of arm motion demands an optimal coordination between the scapula and humerus in order to maintain the congruence of the humeral head into the glenoid cavity [START_REF] Kibler | Clinical implications of scapular dyskinesis in shoulder injury: the 2013 consensus statement from the 'Scapular Summit[END_REF]. For the control group, the clavicular orientation ranged between -37 and -26° for the retraction, and 9 and 19° for the elevation. These values were in the same range of motion than those reported by [START_REF] Myers | Scapular position and orientation in throwing athletes[END_REF]. The scapular orientation in our control group ranged between 35 and 38° for internal rotation, -8 and 44° for upward rotation, and -2 and 10° for anterior tilt. These patterns during scaption in our control group were similar to those reported in the literature for healthy persons [START_REF] Ludewig | Motion of the shoulder complex during multiplanar humeral elevation[END_REF]). We then assumed that the differences in clavicular and scapular kinematics observed between swimmers and controls were related to swimming practice.

Regardless of their specialty, swimmers are known to present a forward posture with a forward head and rounded shoulders [START_REF] Laudner | Forward Shoulder Posture in Collegiate Swimmers: A Comparative Analysis of Muscle-Energy Techniques[END_REF][START_REF] Hibberd | Comparison of Upper Extremity Physical Characteristics Between Adolescent Competitive Swimmers and Nonoverhead Athletes[END_REF].

Whatever age or skill-level, our swimmers presented similar adaptations as attested by the increased clavicular protraction in comparison to controls. However, this adaptation was less in adult elite swimmers when compared to adolescent elite or adult club-level swimmers, which may be explained by the strength and conditioning training performed for prevention of shoulder injury [START_REF] Bak | The practical management of swimmer's painful shoulder: etiology, diagnosis, and treatment[END_REF]. Such training may compensate the forward posture in developing strength of the posterior shoulder musculature (Van de Velde, De [START_REF] Van De Velde | Scapularmuscle performance: two training programs in adolescent swimmers[END_REF], as well as in stretching the anterior shoulder musculature [START_REF] Gaunt | Soothing suffering swimmers: a systematic review of the epidemiology, diagnosis, treatment and rehabilitation of musculoskeletal injuries in competitive swimmers[END_REF]. Contrary to our initial hypotheses, our swimmers did not present increased clavicular elevation when compared to controls. In our study, shoulder kinematics was evaluated up to 120° of humeral elevation, while the hand entry for freestyle requires an arm elevation of 150° [START_REF] Du | Three dimensional motion of shoulder complex during front crawl swimming[END_REF]. The lack of clavicular kinematic adaptations until 120° of humeral elevation may not augur any adaptations for higher humeral elevation.

The forward shoulder posture has been previously associated to an increased scapular internal rotation and anterior tilt, and a decreased scapular upward rotation in a healthy adult population [START_REF] Kebaetse | Thoracic position effect on shoulder range of motion, strength, and three-dimensional scapular kinematics[END_REF], which is quite different from the adaptations in scapular kinematics observed in our swimmers. Indeed, whatever the age and skill-level, our swimmers presented similar dominant scapular upward rotation than controls, while the swimmer's nondominant scapulae were more upwardly rotated when the humerus elevated until 120° in comparison to controls. Such an adaptation may be beneficial to preserve the clearance of the acromial space at the non-dominant side [START_REF] Forthomme | Scapular positioning in athlete's shoulder : particularities, clinical measurements and implications[END_REF], and may minimize the risk for subacromial impingement syndrome [START_REF] Laudner | Forward Shoulder Posture in Collegiate Swimmers: A Comparative Analysis of Muscle-Energy Techniques[END_REF]. The similar bilateral upward rotation positioning of both the scapulae up to 120° of humeral elevation observed in our study were in line with previous results assessing scapular upward rotation in static arm elevation at 90 and 140° in a large group of adolescent swimmers (McLaine, Ginn et al. In Press). Our findings revealed that the elimination of the side-to-side differences in scapular upward rotation in swimmers occurred during dynamic humeral elevation, which may be explained by the symmetrical nature of swimming [START_REF] Mckenna | Differences in scapular and humeral head position between swimmers and non-swimmers[END_REF]. For sport and clinical assessments, no bilateral differences in scapular upward rotation during dynamic humeral elevation up to 120° in the scapular plan may be a significant outcome for shoulder injury prevention (McLaine, Ginn et al. In Press). Contrary to our initial hypothesis, scapular tilt was not altered by swimming exposure. The absence of adaptation in scapular anterior/posterior tilt may be explained by the intra-group variability, especially in our control group, and/or by the error of measurement in relation with measurements using electromagnetic system [START_REF] Karduna | Dynamic measurements of three-dimensional scapular kinematics: a validation study[END_REF]. Concerning the last degree of freedom of the scapula, only the adult elite swimmers presented increased scapular internal rotation, especially at humeral elevation near 120°, suggesting that such adaptation would be generated by the accumulation of years of swimming practice at high level. Consequently, swimming may have differential effect on adaptations in scapular kinematics.

Our study displays some limitations that warrant discussion. A first limitation concerns the lack of a group composed of club-level adolescent swimmers, which would allow the assessment of the interaction effect of age and skill-level. Therefore, it was assumed that comparison between adult club-level (G3_AduClub) and adult elite (G2_AduElit) groups revealed the effect of skilllevel, while the comparison between adolescent (G1_AdoElit) and adult elite (G2_AduElit) groups gave the effect of age. A second limitation was that only men were enrolled in this study.

Therefore, future studies with larger sample should also focus on women to assess a possible sex effect on scapular adaptations in swimmers. A third limitation was that the data was not collected in water, yet different adaptations could have been observed in such environment.

Nevertheless, no current instrumentation allows accurate measurements of the scapula in water condition [START_REF] Pink | The normal shoulder during freestyle swimming. An electromyographic and cinematographic analysis of twelve muscles[END_REF]. Despite these limitations, the present study is the first to assess the shoulder and scapular kinematics throughout the arm elevation in the scapular plane to address the shoulder sport-specific adaptations in swimmers. It could be useful to include scapular kinematics measurements in a follow-up study to better understand how such scapular adaptations occur during the swimmer's career. Further studies also need to determine the influence of preferred swimming style on the shoulder and scapular kinematics, as well as to investigate the shoulder and scapular kinematics during dynamic humeral elevation in swimmers with symptomatic shoulders in order to understand the mechanisms leading to shoulder pathology.

Conclusion

This study confirmed that, in the context of humeral motion up to 120° in the scapular plane, swimmers presented forward posture evidenced by clavicular protraction. Our results also pointed out that bilateral differences in scapular upward rotation were eliminated in swimmers, suggesting safe adaptations of their non-dominant shoulder. In addition, the adaptations in scapular internal rotation may be due to the accumulation of years of practice at high level.

Finally, the findings of this study provide new knowledge on the adaptations in shoulder and scapular kinematics in relation with the age and level of swimming. In particular, focusing on clavicular retraction, scapular external rotation and bilateral symmetry in scapular upward rotation during humeral elevation may be objectives for swimming coaches and physicians to better prevent and rehabilitate shoulder injury in swimmers. Nevertheless, further studies are needed to assess the relationship between scapular kinematics and shoulder injuries in swimmers of different ages, style preference and levels.

Figure 1 -

 1 Figure 1-Clavicular and scapular orientations

Figure 2 -

 2 Figure 2-Mean protraction/retraction with respect to the humerothoracic elevation for G0_Cont (black solid line), G1_AdoElit (grey dashed line), G2_AduElit (black dashed line), and G3_AduClub (black dotted line).# means a significant difference between G0_Cont and G1_AdoElit at p<0.05 inside the grey shaded zone † means a significant difference between G0_Cont and G2_AduElit at p<0.05 inside the grey shaded zone * means a significant difference between G0_Cont and G3_AduClub at p<0.05 inside the grey shaded zone § means a significant difference between G2_AduElit and G3_AduClub at p<0.05 inside the grey shaded zone ‡ means a significant difference between G2_AduElit and G1_AduClub at p<0.05 inside the grey shaded zone

Figure 3 :

 3 Figure 3: Mean internal/external rotation of the scapula with respect to the humerothoracic elevation for G0_Cont (black solid line), G1_AdoElit (grey dashed line), G2_AduElit (black dashed line), and G3_AduClub (black dotted line).† means a significant difference between G0_Cont and G2_AduElit at p<0.05 inside the grey shaded zone ‡ means a significant difference between G2_AduElit and G1_AduClub at p<0.05 inside the grey shaded zone § means a significant difference between G2_AduElit and G3_AduClub at p<0.05 inside the grey shaded zone

Figure 4 :

 4 Figure 4: Mean (thick line) ± 1 standard deviation (shaded zone) downward/upward rotation of the scapula with respect to the humerothoracic elevation for the dominant (blue) and nondominant side (red). G0_Cont: top left, G1_AdoElit: top right, G2_AduElit: bottom left, and 3_AduClub bottom right. ⁑ denotes a significant difference between the dominant and nondominant side (p<0.05).

Table 1 :

 1 Characteristics of the four groups.

		G0_Cont	G1_AdoElit	G2_AduElit	G3_AduClub
	n	11	11	10	10
	Age (years)	23.2±1.7	17±1.0 #	21.9±2.2	20.8±4.4
	Height (m)	1.73±0.10	1.86±0.07 # ‡	1.84±0.06 # ‡	1.76±0.07
	Mass (kg)	68.2±13.5	71.1±7.1	76.9±8.7	69.2±11.1
	Quotation (points)	0.0±0.0	1192±59 # ‡	1248±83 # ‡	1009±138 #
	Swimming Experience (years)	0.0±0.0	10.5±2.3 #	13.9±5.1 # †	13.7±4.7 # †
	Training/week (h)	NA	17.9±3.3 ‡	15.5±4.6 ‡	8.1±4.4

# different from the control group (G0_Cont) at p<0.05 ‡ different from the adult club-level group (G3_AduClub) at p<0.05 † different from the adolescent elite group (G1_AdoElit) at p<0.05

Acknowledgments none