Clinical and Imaging evaluation of rotator cuff tendons in Elite Waterpolo player

Background: Rotator cuff structural changes are common in overhead throwing athletes, such as baseball, javelin, swimming, volleyball, by increasing the risk of shoulder pain and injury. The structural alterations in elite waterpolo players are not well known. In elite waterpolo athletes there are structural alterations of rotator cuff tendons due to overuse of the dominant shoulder compared to the nondominant, like in other overhead disciplines, identiable by ultrasound (US). Methods: Asymptomatic elite men waterpolo players were selected. All athletes were evaluated with standardized scales of shoulder pain and function (Oxford Shoulder Score, Constant Shoulder Score) and provided data of training, injury and shoulder pain history. Each athlete underwent clinical evaluation of shoulders followed by US of rotator cuff, biceps and bursas. Results: Twenty-three athletes met the inclusion criteria, mean age 24.2±3.3. Fourteen athletes (61%) presented higher degeneration grade at the dominant supraspinatus compared to the contralateral, always in the same area in outeld players: anterior, lateral, pre-insertional. In twenty-two (95%) the biceps tendon was damaged: Twenty athletes (87%) bilaterally, two (9%) at the only dominant limb. The site was always at the bicipital groove in its insertion on the humerus. Power Doppler (PD) evidenced neovascularization in only ve (22%) players at supraspinatus: four bilaterally, one only at the nondominant. No statistical correlation was found between tendon degeneration and age, career years. Conclusion: Outeld waterpolo players have peculiar changes in supraspinatus at level, as seen in other overhead throwing athletes. We found changes also in biceps, bilaterally, like in shoulders of elite swimmers. We suppose that these changes are predictive of shoulder pain and injury.

Because of the coexistence of swimming, throwing the ball and contacts among players, it is supposed that shoulder injuries are common in waterpolo players too [13,14]. In literature there are only two papers carried out in high-level waterpolo players but Jerosh et al. in 1993 and Galluccio et al. did not nd any difference between dominant and non-dominant shoulder [14,15].
The aim of this study is to evaluate, clinically and with US, shoulders of asymptomatic high-level waterpolo players at the beginning of the season.
The hypothesis of this study is that in elite waterpolo athletes there are some structural alterations of rotator cuff tendons due to overuse of the dominant shoulder compared to the non-dominant, identi able by US.

Methods
The study included asymptomatic elite male waterpolo athletes from the three teams in Lombardy participating at Italian Premier League and attending without any restriction at all trainings, practices, matches. After providing informed consent, each player completed a questionnaire with age, sex, hand dominance, numbers of years training, training volume, his history of throwing shoulder injury, and demographic data. Exclusion criteria included shoulder injury or pain requiring treatment, systemic musculoskeletal diseases, current use of non-steroidal anti-in ammatory drugs (NSAIDs) or steroids and metabolic, rheumatic, osteoarticular or neoplastic diseases. Injury data were then con rmed from the medical record of the team. Our examination was performed before the beginning of the regular season and the study protocol was approved by the institutional review board of our Hospital. Each player received an independent physical examination of both shoulders performed by an orthopaedic shoulder surgeon (M.R.) and completed the Oxford Shoulder Score and Constant Shoulder Score [16]. Players with Oxford Shoulder Score value ≥40 and Constant Shoulder Score value <11 were enrolled. The dominant and non-dominant shoulders were examined by a single musculoskeletal radiologist (L.C.), with 30 years of experience in performing shoulder ultrasound, according to the protocol described by the European Society of Musculoskeletal Radiology [17], as described in Figure 1A and 1B. A Grayscale US with 7.5-MHz high resolution linear probe (frequency 350 MHZ) with longitudinal and transverse scans, was performed.
Sportsmen and the radiologist were blinded to the hand dominance throughout data collection.
The area of the tendon degeneration was the same in twenty athletes (87%): anterior, lateral, preinsertional. Only in the two goal-keepers and in one out eld player it was different: posterior and medial (P<.05). Power Doppler evidenced neovascularization in ve (22%) players at supraspinatus: four bilaterally, one only at the non-dominant ( Figure 2B). No neovascularization in all the players at subacromial bursa and subscapularis tendon. One athlete had PD positivity at biceps (Table 3). In six (21%) athletes was found degeneration at the subacromial bursa at the dominant limb, four (17%) at the non-dominant limb, two (9%) bilaterally. Thirteen players (56%) had no structural alteration bilaterally (P≥.05). In seven patients (30%), ultrasound evidenced associated supraspinatus and subacromial bursa damage: four at only the dominant shoulder, three at only the non-dominant (P≥.05). n.s a n.s a n.s a n. In seven players (30%) was observed a grade ≥1 subscapularis tendon degeneration at the only dominant limb, two (9%) at the only non-dominant, one (4%) bilateral degeneration (P≥.05) ( Table 3). The damage zone was observed near the insertion on the lesser humeral tuberosity (P<.05). In twenty-two athletes (96%) the long head of biceps tendon was damaged: twenty athletes (87%) bilaterally, two (9%) at the only dominant limb (P<.05). Only one patient had no alteration in this structure (Table 3). In all the athletes analyzed the site of alteration was the same: at the bicipital groove in its insertion on the humerus (P< .05). No statistical correlation was found between tendon degeneration and age, career years.

Discussion
Waterpolo is a contact sport which also provides a shooting and a swimming phase and this aspect implies a major stress on the shoulder [21]. It is assumed that in elite athletes repeating technical movements induces structural alterations of the stabilizing components of the shoulder, as already observed in studies performed on other overhead athletes [1,6]. Studies have been performed related to the shooting mechanics of the baseball pitchers and the relative injury risk from shoulder overuse [3,6].

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The throwing biomechanics in waterpolo is similar to baseball but there are important differences: the dimensions and weight of the ball, the lack of a solid base during throwing phase. These characteristics in uence the angular acceleration of the elbow and cause a decrease of the throwing speed [22]. In literature, there are few data regarding changes of the rotator cuff in waterpolo [23]. Previous authors have demonstrated that US and MRI have comparable and high accuracy for detecting full-and partial thickness tears in rotator cuff [24][25][26]. MRI gives more information about muscle degeneration, the under acromion area and other coexisting pathologic process. We chose ultrasound because it is dynamic, less invasive and more sensitive than MRI in assessment of rotator cuff pre-insetional tendinopathy. Other studies carried out in volleyball, basketball, baseball and swimmers used US to evaluate the rotator cuff tendinopathy [1,[24][25][26][27].The international protocol proposed by European Society of Musculoskeletal Radiology (ESMR) was adopted because considered as the most detailed and effective protocol for analysis and the comparison with other overhead-throwing studies [17]. 61% of patients had a higher degeneration of the dominant supraspinatus compared with non-dominant (P< .05). In the 87% of athletes, the location of the tendon degeneration was anterior, lateral and pre-insertional, like in baseball and volley ball players (P< .05). All were out eld players. In the two goal-keepers the degeneration was bilateral, symmetrical and in a different position: posterior and medial. We suppose that this difference is due to the activities performed by goalkeepers that are not the same of out eld players: the goalkeeper makes rarely high energy shots on goal, but often performs slow passages at variable distance not exceeding 20 meters. During the defensive phases the upper limbs of the goalkeeper are both raised to defend the goal area or move simultaneously underwater, increasing the leg thrust to reach the extreme limits of the goal. In the sessions of swimming, unlike out eld players who practice predominantly freestyle, the goalkeeper performs predominantly butter y. Like in other studies, no statistically signi cant difference in tendon diameter was found between dominant and non-dominant supraspinatus [2,28,29]. The more stressed structure in the waterpolo throwing technique is the supraspinatus tendon, like in other overhead throwing disciplines [1,5,6,8,29]. Nine athletes (39%) had bilateral grade ≥1 supraspinatus degeneration because also non-dominant shoulder is stressed during swimming phases [23]. The statistical analysis evidenced that among the variables studied, structural degeneration is the most in uential to de ne the difference between the tendons of the shoulder. Ocguder et al. evidenced that, in overhead sports, supraspinatus tendon is overloaded, with its bursa [28]. In our study, the supraspinatus alteration is associated with bursa in only 30% of cases and without a relevance in dominant or non-dominant arm. Subacromial bursa is low stressed in our study. We suppose that this difference is due to the time when we analyzed the athletes, at the beginning of the season. This difference into overhead disciplines is probably due also to a different shoot dynamic, heavy and measures of the ball, friction with the water, absence of xed support. This induces a displacement of the vector sum of forces at the level of stabilizing structures of the shoulder, resulting in an increased stress at these level [22]. The subscapularis tendon is less stressed in overhead sports, like described in other works in this study, therefore we analyzed the tendon echotexture and not the diameter [1,2,4,15,27]. Only eight (35%) of the evaluated athletes had a tendon degeneration ≥1 at the dominant subscaularis.
No difference of subscapularis degeneration between the two limbs con rms a predominant involvement of this tendon in swimming and less in the throwing phase [6]. The LHB in the water polo player, unlike what is observed in the other overhead throwing disciplines, is very stressed [4,30]. In the 96% of the cases a degeneration has been observed, 91% bilaterally. The area of the degeneration was for every athlete the same, where the tendon goes into the biceps pulley (P<.05). It can be assumed that this tendon is involved especially during the swimming phases, as seen in the study of Rodeo et.al in swimmers, who noted biceps tendinosis in 72% of the analyzed shoulders [6,31]. Previous studies have shown that the severity of the tendon degeneration shoulder would correlate with the number of trainings per week, career years, the role and of course with any work activity that the athlete engages outside the pool. In this study, as in many others carried out on athletes, ages and years of activity were not in uential [32]. Ultrasound examination was completed for each patient with power doppler: previous studies, carried out mainly on Achilles and patellar tendons in marathon runners, footballers and volleyball players, have shown a variation of the local tendon vascularity associated with the increase of activity and have identi ed a data correlation with risk of injury during the course of the season. PD was de ned as a predictive method for future pain and injuries [33][34][35]. At the beginning of the season PD has shown low percentage of vascularity. Our next goal is to assess new PD evaluation at the end of the season and correlate the vascularity status with symptoms. Our hypothesis is that PD can have a predictive value of shoulder pain also for rotator cuff tendons. Strength points of our study are the careful high level water polo player selection: asymptomatic, no previous surgery or accident, no intraperirticular in ltration. The US was performed at the beginning of the season, when tendon stress was low. The radiologist had 30 years of experience in shoulder ultrasound examination. It has been a singleblind evaluation: dominant arm, age, position, career years of the athletes were unknown to the radiologist. The study limits are the low number of chosen athletes: in Lombardy there are three Italian Premier League teams, composed by average 13-15 athletes in each team. The goal-keeper number is very low compared with movement players: a waterpolo team is composed by fteen athletes, with only two goal-keepers. Left-handed players number is lower than right-handed: this aspect characterize also daily life. In a water polo team, usually there are one or two left-handed athletes.

Conclusion
Our study shows a high prevalence of structural changes in supraspinatus tendon in asymptomatic elite water polo players. Out eld players have peculiar changes in supraspinatus at pre-insertional level, as seen in other overhead throwing athletes. In goal-keepers supraspinatus degeneration is bilateral and located more medially and posteriorly. We found changes also in biceps tendon, bilaterally, like in shoulders of elite swimmers. We suppose that these changes are predictive of shoulder pain. Our perspectives are to follow the athletes, clinically and with ultrasound, to demonstrate our hypothesis and draft more players. The study design was approved by the Insubria University ethics committee. An informed verbal consent by each athlete to participate to this study was obtained. We took only verbal consent because no invasive intervention was performed and athletes were enrolled with scienti c purpose. At the beginning of the enrollment they should complete two clinic selection questionnaires (Oxford Shoulder Score and Constant Shoulder Score) and we considered these as a written consent.

Consent to publish
At the time of enrollment it was clearly speci ed our scienti c objective to publish the manuscript on a sport medical journal. Every athletes enrolled gave his verbal consent. However images in our manuscript are entirely unidenti able and there are no details of individuals reported.
No funding was received in the development of this study, but only passion for a sport associated with passion for our job.
Authors' contribution Author 1: AR (Medical Resident) andrea.ruberti5@gmail.com: enlisted the patients, collected the clinical data, got informed consent, contributed analysis tools, performed the analysis of data with the help of MR and wrote the paper. 1A-1B: Ultrasonographic technique. The arm of the athlete brought posteriorly, placing the palmar side of the hand on the superior aspect of the iliac wing with the elbow exed and directed posteriorly. The supraspinatus tendon was evaluated along its long and short-axis. Rotate the arm externally xing the elbow on the iliac crest to show the subscapularis tendon and its insertion on the lesser tuberosity. The biceps tendon was examined placing the arm in slight external rotation (directed towards the contralateral knee) with the elbow exed 90°, palm up. Shift the probe up to examine the biceps in its intra-articular course with the bicipital groove and down to reach the myotendinous junction. Moving the probe toward medial on transverse planes, look at the coracoid process, the coraco-acromial ligament, the conjoined tendon and the anterior aspect of the subacromial bursa [17].