Liaghat2018 PDF
Liaghat2018 PDF
PII: S1050-6411(17)30364-4
DOI: https://doi.org/10.1016/j.jelekin.2018.01.003
Reference: JJEK 2153
Please cite this article as: B. Liaghat, B. Juul-Kristensen, T. Frydendal, C. Marie Larsen, K. Søgaard, A. Ilkka Tapio
Salo, Competitive swimmers with hypermobility have strength and fatigue deficits in shoulder medial rotation,
Journal of Electromyography and Kinesiology (2018), doi: https://doi.org/10.1016/j.jelekin.2018.01.003
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Competitive swimmers with hypermobility have strength and fatigue deficits in shoulder
medial rotation
Behnam Liaghata,b, Birgit Juul-Kristensena, Thomas Frydendala, Camilla Marie Larsena,c,, Karen
a
Department of Sports Science and Clinical Biomechanics, University of Southern Denmark,
Odense, Denmark, bDepartment for Health, University of Bath, Bath, United Kingdom, cHealth
Corresponding author
Thomas Frydendal, Physio- and Occupational Therapy, Lillebaelt Hospital – Vejle, Beriderbakken
Camilla Marie Larsen, Department of Sports Science and Clinical Biomechanics, University of
Karen Søgaard, Department of Sports Science and Clinical Biomechanics, University of Southern
Aki Salo, Department for Health, University of Bath, Applied Biomechanics Suite 1.309, Claverton
1
1. Introduction
passive system due to ligamentous or capsular looseness. The condition implies increased risk of
traumatic and non-traumatic shoulder dislocations (Cameron et al., 2010; Chahal et al., 2010), and
is a risk factor for overuse shoulder injuries (Zemek & Magee, 1996). The reason for this is not yet
known, but is probably due to decreased strength, muscle activity and coordination, and eventually
increased fatigue. Decreased isokinetic strength has been found in children and adults with
symptomatic and non-symptomatic GJH and knee hypermobility (Juul-Kristensen et al., 2012). In
contrast, recent studies of children with non-symptomatic GJH showed no reduced maximum
isometric knee strength and hop length (Jensen et al., 2013; Junge et al., 2015). In fact, these
studies reported that individuals with GJH use altered or compensatory muscle activation strategies
in both agonist and stabilizing leg muscles. To our knowledge no studies have reported shoulder
strength and muscle activity in individuals with GJH including hypermobile shoulders (GJHS).
(Borsa et al., 2000), glenohumeral instability and/or increased risk of recurrent joint luxation
(Cameron et al., 2010; Chahal et al., 2010). In this aspect, previous findings indicate that these
individuals present more precisely with altered muscle activity of scapular stabilisers and rotator
cuff muscles (Barden et al., 2005), decreased shoulder muscle strength (Edouard et al., 2011),
scapular function (Struyf et al., 2011) and shoulder proprioception (Laudner et al., 2012). In line
with studies on MDI, it can be hypothesised that individuals with GJHS have functional deficits
and altered muscle activity in the shoulder; however, this remains scientifically unanswered.
Young competitive swimmers represent a group with high prevalence of GJHS (Junge et
al., 2016). This may be due to the demand of a greater range of shoulder motion to achieve a body
position that reduces drag and increases stroke length, which ultimately results in better swimming
performance (Wanivenhaus et al., 2012). Having GJHS in addition to being exposed to repetitive
shoulder rotation movements during competitive swimming, these individuals may be predisposed
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to muscle-tendon overload, muscle fatigue and pain. Thus, the aim of this study was to investigate
whether young competitive swimmers with GJHS have reduced shoulder strength, increased
isokinetic fatigue development and altered muscle activity during swimming-related movements of
shoulder rotation.
2. Methods
This study was cross-sectional comparing 13-17 years old competitive swimmers (highest national
level) with GJHS and control swimmers without GJHS, individually matched on age, sex and
swimming club. Participants were recruited from local sports clubs by initial email and phone
contacts with coaches and parents. Study procedures were approved by the Research Ethics
Approval Committee for Health at the University of Bath (EP 14/15 175). Participants and their
Data were collected during two sessions: (i) the screening session consisting of clinical tests for
the principal investigator to the participants’ health status (controls or GJHS); and (ii) the test
another day.
An element of shoulder laxity and GJHS is seen in many competitive swimmers, and both a
combination of acquired and inherent factors contribute to shoulder laxity in swimmers. Due to the
study design the included swimmers had to be inherently joint hypermobile and not only present
with acquired hypermobility due to the swimming exposure, hence the Beighton tests for GJH were
used during the screening session. Beighton tests have been found reproducible for testing GJH
(Juul-Kristensen et al., 2007) and include nine tests: apposition of the thumbs, hyperextension of
elbows and knees, dorsalflexion of the fifth fingers, all bilaterally, and forward bending in
standing. Each positive test scores one point with nine points being the highest possible score.
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Since the Beighton tests do not specifically include the shoulder joint, a shoulder test included in a
Spanish test battery (Rotes-Querol, 1957) for GJH was added to ensure shoulder hypermobility.
The test was shoulder lateral rotation (positive score >90°) with the upper arm in neutral along the
side of the body, previously found to have satisfactory reliability (Juul-Kristensen et al., 2007).
The group with GJHS was defined with Beighton score ≥5 (Juul-Kristensen et al., 2007),
and positive shoulder hypermobility in at least one shoulder. Inclusion criteria for controls were a
Beighton score ≤3 and no shoulder hypermobility. Further inclusion criteria for both groups were:
being swimmer, having normal training and competition activity within the latest seven days, and
being matched for age and sex. Exclusion criteria were previous serious trauma to the upper
During the actual test session, the participants firstly answered questionnaires about
training activity, competitive swimming, other sports activities, previous injuries, perceived
shoulder instability by the Western Ontario Shoulder Instability Index (WOSI) questionnaire and
pain intensity measured by pain rating on Visual Analogue Scale (VAS) for current pain, pain
during the latest 24 hours, and pain during the latest seven days (Table 1). Subsequently,
information on anthropometric data was collected followed by the EMG electrode placement
procedure. Then the participants completed a standardised warm up program for 10 minutes,
comprising unilateral and bilateral shoulder movements (10 repetitions of flexion, extension,
horizontal abduction and adduction), scapular protractions against a wall, and standing push-ups
against a 90-cm high table, followed by simultaneous EMG recordings during maximum voluntary
isometric contraction (MVIC) tests, and isokinetic measurements. After the isokinetic testing
The isokinetic concentric shoulder medial and lateral rotation measurements were
performed on a calibrated Cybex NORM dynamometer (Cybex Inc., Ronkonkoma, New York,
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USA) with the dominant arm defined as the side used for handwriting. One swimmer had GJHS on
his non-dominant shoulder, in which case the non-dominant shoulder was tested on him and his
matched control. The test position was selected to be close to the freestyle swimming stroke. The
participants were prone lying with 90° shoulder abduction and 90° elbow flexion (Figure 1), and
were fixated with belts around the mid lumbar spine and 10 centimetres above knee level. Centre of
rotation for the shoulders were placed to be in line with the rotation arm of the dynamometer. To
minimise risk of injuries in end range, total range of motion was set to 95°, ranging from 35° of
Five repetitions of maximum shoulder rotation strength were performed at 60°/s, and 10
repetitions at 180°/s, with 60 seconds of rest periods between each test, and the current velocities
were selected as those most similar to the estimated velocities performed during swimming (Bak &
Magnusson, 1997). Before each test, participants had five trials to familiarise with movements and
velocities. No visual feedback was allowed, however, participants were encouraged to perform
maximally with verbal instructions. Outcome measures were peak torque (the maximal value of the
moment angle position curve) and maximum work (the repetition with highest value in torque x
angular displacement) for both directions at both velocities (60°/s and 180°/s) normalised to body
mass. Fatigue development in isokinetic strength was calculated as the decrease in work
2.3 Electromyography
During isokinetic testing, surface EMG (Telemyo DTS, Noraxon Inc. Scottsdale, USA)
was measured in the scapular stabilising muscles (mm. upper trapezius, lower trapezius and
serratus anterior), the primary medial rotation agonist (m. pectoralis major), and the primary lateral
rotation agonist muscle (m. infraspinatus). Once the exact point for electrode placement attachment
was identified, the skin was lightly shaved, rubbed and cleaned with alcohol to keep skin
impedance lower than 10 kOhm, measured with a digital multimeter. Bipolar electrodes (Ag/AgCl,
5
Ambu Blue Sensor, N-00-S/25, Ballerup, Denmark) were attached to the skin with a two-
centimetre inter-electrode distance, and in line with muscle fibres. The locations of electrodes were
as follows: upper trapezius, 20% medial to the mid distance between seventh cervical vertebra and
acromion’s lateral border (Holtermann et al., 2009); lower trapezius, 33% medial to the midpoint
between the medial border of the scapula and eighth thoracic vertebra (Holtermann et al., 2009);
serratus anterior, at the seventh rib, below the axilla, posterior to pectoralis major and anterior to
latissimus dorsi (Holtermann et al., 2010) in line with the xiphoid process and the axillary border;
infraspinatus, two and a half cm distal to the centre of the scapular spine (Barden et al., 2005);
pectoralis major, one third of the distance from tuberculum major to the xiphoid process (Pontillo
et al., 2007).
For each muscle, maximum voluntary electrical activity (MVE) signal was recorded during
MVIC in standardised anatomical positions. Upper trapezius was tested in standing with the arm in
90° elevation in scapula’s plane with the thumb pointing upwards, while performing elevation. For
serratus anterior, a similar testing position was used with the arm elevated to 135°. Lower
trapezius was tested in prone with the arm in 125° of abduction along muscle fibres, performing
horizontal abduction. Infraspinatus was tested in prone lying with the arm in 90° of abduction and
the elbow in 90° of flexion during performance of shoulder lateral rotation, and pectoralis major
was tested in supine lying with 90° of shoulder flexion during horizontal adduction performance.
An external load of 40 kg was used for resistance, and to stabilise the body a manual isometric
resistance was applied on the non-measured arm while the participants were fixated with belts in
the prone and supine lying positions. A total of three sets, with each contraction lasting five
seconds, were performed with 60 seconds rest period between each set.
Three clinical tests for glenohumeral instability were used, including Gagey hyperabduction, sulcus
and load-and-shift tests. The Gagey hyperabduction test for the inferior glenohumeral ligament was
6
considered positive with shoulder abduction beyond 105° (Gagey & Gagey, 2001). For the sulcus
test, multidirectional instability was defined as more than two centimeters widening between
acromion and the humeral head (Neer & Foster, 1980). In the load-and-shift test, severe ventral or
dorsal glenohumeral instability was defined as grade two or three (i.e. humeral head moved beyond
the glenoid labrum, and was relocated spontaneously or remained dislocated), on a scale from 0-3
Raw EMG signals were amplified with gain 500 and bandpass filtered with 10-500 Hz
(Noraxon Inc. Scottsdale, USA). The analogue signal was recorded on a computer via laboratory
interface (CED Power 1401 16 bit, Spike2 software, Cambridge Electronic Design Limited, UK)
with analogue to digital converting at 1000 Hz. For medial and lateral rotation, muscle analyses
were performed with custom-made software (Hedera 3.0, The University of Southern Denmark). In
EMG signals, changed shoulder rotation directions were marked by triggers defining start/stop of
each medial and lateral rotation movement. EMG signals of each muscle during peak torque and
maximum work repetitions were normalised to the respective muscle’s MVE, defined as the
highest Root Mean Square (RMS) amplitude in a moving window of 100 ms across the whole
Baseline variables were tested for normality (Shapiro-Wilk, histograms and QQ-plots), and found
to be normally distributed except for pain intensity and WOSI. For demographic data, un-paired t-
tests were used to test for group differences on continuous data (Beighton score, age, height, body
mass, swimming competitive experience, swimming during practice and other sports activities),
while Mann-Whitney was used for non-normal data (pain intensity and WOSI), and Fisher’s exact
test for dichotomous data (Rotes-Querol and glenohumeral instability tests). For between-group
differences in the outcomes of peak torque, maximum work and %MVE, a linear regression model
was estimated adjusting for gender, age and body mass, without violating the assumption of
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normality. For isokinetic fatigue (J/repetition) calculations during repetitions from 2-10 at 180°/s, a
linear regression mixed effect model was applied with age, gender and body mass as covariates,
using ID number as random factor. For the isokinetic fatigue development, a negative coefficient
Sample size was calculated to be minimum 16 per group based on previous isokinetic
values (Bak & Magnusson, 1997), with estimated standard deviation and minimum mean
difference of 0.10 Nm/kg and 0.07 Nm/kg , respectively, with = 0.05 and =0.20. To
accommodate for drop-outs, 19 participants per group were recruited, however, there were no drop-
outs. P-values <0.05 were reported as statistically significant, while tendencies to significance were
defined as p-values >0.05 <0.10. All statistical analyses were performed using STATA (StataCorp,
2015, Stata Statistical Software: Release 14. College Station, TX: StataCorp LP.)
3. Results
In total, 97 competitive swimmers were screened for eligibility, of which 38 swimmers, 11 girls
and eight boys in each group, completed the study. The groups were comparable on demographics
(age, height, body mass, sports participation, previous and current pain levels, WOSI and clinical
tests for shoulder instability) except for the Beighton and Rotes-Querol tests, as expected due to the
0.60 Nm/kg; p=0.047), and significantly lower (14%) maximum work (0.62 vs 0.71 J/kg; p=0.031)
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3.2 Isokinetic fatigue
Based on linear regression models, swimmers with GJHS showed significantly larger isokinetic
fatigue development in medial rotation at 180°/s (-0.257 vs 0.064 J, SE=0.088; p=0.010) with a
between groups difference in time effects of 0.321 J/Repetition (SE= 0.124). There were no
There were tendencies to lower %MVE (20%) for GJHS swimmers in infraspinatus in peak torque
(60°/s medial rotation) (29.1 ± 10.6 vs. 35.5 ± 11.4 %MVE; p=0.066), and lower %MVE (34%) in
maximum work in pectorals major (30.0 ± 22.1 vs. 42.3 ± 25.8 %MVE; p=0.092), but generally
4. Discussion
Swimmers with GJHS, despite having no formal diagnosis, displayed both lower isokinetic peak
torque and maximum work in medial rotation at 60°/s, and larger fatigue development in isokinetic
strength during medial rotation strength measurements at 180°/s. There were no significant group
Velocities under 120°/s have been defined as those corresponding to strength (the amount
of force muscles can exert against an external load), while higher velocities such as 180 °/s have
been defined as corresponding to power (the ability to generate as much force and as fast as
possible) (St. Pierre et al., 1984). The significantly lower isokinetic performance at 60°/s (12-14%)
indicates that participants with GJHS lacked muscle strength rather than power. The lower medial
rotation strength in comparison (and no group differences in lateral rotation strength) was an
interesting finding, because the medial rotation movement is one of the main propulsive
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movements throughout the acceleration phase in swimming strokes. In fact, up to 4000 strokes per
day in medial rotation with each arm are performed by high-level competitive swimmers (Bak &
Faunø, 1997). These findings suggest that swimmers with GJHS could exert less force during the
isokinetic test due to the musculoskeletal impairment itself, with the inclusion criteria of an
external shoulder rotation of more than 90°. Similar sized strength deficits in GJH (ranging from
18-19%), however, in knee strength, were found in 10-year old girls and women with GJH and
knee hypermobility (Juul-Kristensen et al., 2012). Since these two studies differ with respect to
body regions and athletic status (competitive swimmers vs non-athletes), comparison should be
made with caution. The reduced strength in the current study (12-14%) is in line with previous
studies of elite swimmers with shoulder pain (17.5% reduced medial rotation strength) compared
with those without pain (Bak & Faunø, 1997), and athletes with subacromial impingement (11%
reduced scapular retraction-protraction strength) compared with their non-injured shoulder (Cools
et al., 2004). The ‘safe’ limit of maximum 10% side difference before an increased risk of injuries
has been advocated for knees (Tol et al., 2014). Since the shoulder is anatomically and
biomechanically different from the weight bearing knee, it is unknown whether reduced shoulder
strength within the present level (12-14%) represents a risk factor for future injury development.
However, reduced strength in competitive sport may threaten joint integrity with potentially
detrimental consequences. Further, the present result of lower maximum work suggests that
swimmers with GJHS are weaker during the total range of swimming strokes, which may decrease
swimming propulsion and increase joint stress exposure close to end range.
Swimmers with GJHS further showed significantly larger fatigue development during
isokinetic strength measurements in medial rotation (180°/s). This corresponds with the current
reduced maximum work in medial rotation (60°/s) indicating lower endurance compared with
controls, which may alter swimming strike coordination (Suito et al., 2008) and hence increase the
risk of developing fatigue related shoulder pain (Crotty & Smith, 2000; Matthews et al., 2017). The
current result on shoulder fatigue is in line with previous studies of patients with GJH generally
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showing increased fatigue (Voermans et al., 2010; Scheper et al., 2014), however, the long-term
(impingement, rotator cuff tendinopathy and labral tears), preventive measures to avoid this
development is important. Based on the current results, swimmers with GJHS may benefit from
medial rotation endurance and strength training in addition to lateral rotation strength (Cools et al.,
2015) to prevent such injuries. This may be an important topic for future studies.
It was hypothesised that the group with GJHS would show lower muscle activity in
serratus anterior and lower trapezius indicating muscular imbalance in the scapular stabilisers,
which was not confirmed. There was only a tendency to lower muscle activity in medial rotation in
infraspinatus during peak torque and pectorals major during maximum work. The current results
indicate decreased dynamic stabilisation of the humeral head in the hypermobile shoulder due to
altered length-tension conditions for the medial rotators (which was found) and capsular looseness
(not measured). Although a previous study has shown swimmers with shoulder problems to have
lower activity of serratus anterior than swimmers without pain (Pink et al., 1991), such difference
could not be seen in those with GJHS, probably due to the non-pain population. Generally, a lower
activity of this muscle may influence scapular kinematics negatively by positioning the acromion to
impinge on the rotator cuff, with increased risk for pain development (Cools et al., 2004). Lower
muscle activity during medial rotation has previously been found in individuals with MDI as well
as in individuals with subacromial impingement (Barden et al., 2005; Struyf et al., 2011), and may
suggest altered muscle activation in the shoulders. The deeper lying medial rotator of subscapularis
muscle, which requires needle-EMG for measuring its muscle activity, has also shown significantly
lower muscle activity in swimmers with shoulder pain (Pink et al., 1991). Again, the present
population was pain-free, but may have shown same characteristics as swimmers with shoulder
pain with limited optimal working conditions (pain or altered length-tension conditions) for the
working muscles. However, since the subscapularis muscle activity was not measured in the
current study, its contribution to medial rotation remains unknown. The lack of statistically
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significant group differences in EMG activity may be due to large inter-individual variability (SD
range between 19.5 and 34.6 %MVE), thereby increasing the risk of type 2 error. It is not known
whether a more functional task may have shown a clearer pattern of changed EMG-activity in
GJHS, as seen previously in GJH with knee hypermobility during functional tasks such as balance,
One of the limitations in the current study may be the risk of selection bias since the
inclusion criteria were healthy competitive swimmers without pain, thereby eliminating a potential
effect of pain in GJHS. Although the inclusion criteria did not include instability, large positive
prevalence of at least one of the shoulder instability tests was seen in GJHS swimmers indicating
development, as shown in previous studies, may have been present with higher number of
repetitions and/or faster velocities than the present. This was, however, not chosen to avoid
exposing the current participants to potential injuries during the testing procedure. Another
limitation was increased risk of type 2 error in EMG measurements with large standard deviations
since the sample size was based on group differences in isokinetic variables.
The strengths of the study are the strict inclusion criteria, group similarity in demographics
and the standardised procedures in isokinetic and EMG measurements to ensure reliable data
(Edouard et al., 2011; Seitz & Uhl, 2012). Also, the standardized procedures used in the selected
clinical tests for shoulder instability provide satisfactory reliability (Eshoj et al., 2017). The strict
inclusion criteria of healthy swimmers may also be a strength, since it was possible to study the
clear effect of GJHS in swimmers without pain interference. The study population included 57.9%
girls and 42.1% boys making it possible to generalise data to both genders in contrast to previous
studies on GJH with few or no boys included (Juul-Kristensen et al., 2012; Jensen et al., 2013;
12
5. Conclusion
In conclusion, young competitive swimmers with generalised and shoulder joint hypermobility
(GJHS), despite having no formal diagnosis, displayed both strength and fatigue deficits in medial
rotation, which may be some of the contributing mechanisms for development of shoulder injury.
Whether swimmers with GJHS will benefit from medial rotation strength training and not as per
now only lateral rotation strength as injury prevention is an important topic for future studies.
Acknowledgement
The authors would like to thank Henrik Baare Olsen for technical advice, Tore Bjarnason and Sune
Christensen for assistance in testing the swimmers, University College Lillebaelt in Odense,
Denmark, for their support with recruiting participants, and University of Southern Denmark for
providing facilities and equipment to complete this research project. The project was supported by
the Danish Society of Sports Physiotherapy, who was not involved in the conduction of research or
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Table 1. Demographic variables, (mean ± standard deviation, median [range], or number
(percentage)) for self-reported ratings on pain (VAS), and shoulder-related instability and function
(WOSI), in addition to clinical tests for glenohumeral instability, for swimmers with Generalised
(n = 19) (n = 19)
Pain intensity
VAS 0-100 (mm) pain during latest seven days 2.5 [0-49] 9 [0-49] 0.175
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Table 2. Peak torque (Nm/kg) and max work (J/kg), including mean ± standard deviation, during
isokinetic medial and lateral rotation movements at 60°/s (five repetitions) and 180°/s (10
repetitions), for swimmers with Generalised Joint Hypermobility and shoulder hypermobility
difference) difference)
Peak Torque
°
Nm/kg 60 /s 0.53 ± 0.10 0.60 ± 0.13 0.047* 0.38 ± 0,07 0.40 ± 0.07 0.274
°
Nm/kg 180 /s 0.48 ± 0.09 0.51 ± 0.11 0.323 0.32 ± 0.05 0.33 ± 0.05 0.927
Maximum Work
J/kg 60°/s 0.62 ± 0.12 0.71 ± 0.17 0.031* 0.41 ± 0.10 0.43 ± 0.08 0.373
J/kg 180°/s 0.58 ± 0.11 0.62 ± 0.15 0.236 0.34 ± 0.08 0.35 ± 0.08 0.615
17
Figure 1. Experimental set-up for the electromyographic and isokinetic testing procedure.
Figure 2. Electromyographic activity of upper trapezius (UT), lower trapezius (LT), serratus
anterior (SA), pectoralis major (PM) and infraspinatus (INF) at peak torque (A-D) and maximum
work (E-H), expressed as percentage of maximal voluntary contraction (%MVE), during isokinetic
glenohumeral rotation movements at low (60 °/s) and high (180°/s) velocity, for swimmers with
Generalised Joint Hypermobility and shoulder hypermobility (GJHS) and controls. Bars are means,
and standard deviations are shown as error bars. (*) Tendency to significance, p<0.10.
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Abstract
considered an intrinsic risk factor for shoulder injuries. The aim was to investigate the association
of GJHS with shoulder strength, fatigue development and muscle activity during swimming-related
shoulder rotations. Totally, 38 competitive swimmers (aged 13-17 years) participated, 19 were
competitive swimmers with GJHS and 19 were age, sex and club matched swimmers without
GJHS. Concentric isokinetic force in medial and lateral rotations were measured at 60°/s (5
repetitions) and 180°/s (10 repetitions). Electromyographic activity was measured from upper
trapezius, lower trapezius, serratus anterior, infraspinatus and pectoralis major muscles. Swimmers
with GJHS produced significantly lower peak torque (0.53 vs. 0.60 Nm/BW; p=0.047) and
maximum work (0.62 vs. 0.71 J/BW; p=0.031) than controls during medial rotation (60°/s).
Swimmers with GJHS showed significantly larger isokinetic fatigue at 180°/s (0.321 J/repetition;
p=0.010), and tendencies to lower levels of muscle activity in infraspinatus (20%, p=0.066) and
pectoralis major (34%, p=0.092) at 60°/s during medial rotation. Young competitive swimmers
with GJHS, despite no formal diagnosis, displayed strength and fatigue deficits in medial rotation,
potentially inherent with greater risk of shoulder injury. Whether GJHS swimmers benefit from
adolescent
Disclosure of interest
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