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Accepted Manuscript
Motion of the shoulder complex in individuals with isolated acromioclavicularosteoarthritis and associated with rotator cuff dysfunction: Part 1 – Three-di-mensional shoulder kinematics
Catarina de Oliveira Sousa, Paula Rezende Camargo, Ivana Leão Ribeiro,Rodrigo Bezerra de Menezes Reiff, Lori Ann Michener, Tania Fátima Salvini
PII: S1050-6411(14)00097-2DOI: http://dx.doi.org/10.1016/j.jelekin.2014.04.015Reference: JJEK 1708
To appear in: Journal of Electromyography and Kinesiology
Received Date: 23 December 2013Revised Date: 21 April 2014Accepted Date: 24 April 2014
Please cite this article as: C.d.O. Sousa, P.R. Camargo, I.L. Ribeiro, R.B.d. Reiff, L.A. Michener, T.F. Salvini,Motion of the shoulder complex in individuals with isolated acromioclavicular osteoarthritis and associated withrotator cuff dysfunction: Part 1 – Three-dimensional shoulder kinematics, Journal of Electromyography andKinesiology (2014), doi: http://dx.doi.org/10.1016/j.jelekin.2014.04.015
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Motion of the shoulder complex in individuals with isolated acromioclavicular osteoarthritis and 1
associated with rotator cuff dysfunction: Part 1 – Three-dimensional shoulder kinematics. 2
3
Catarina de Oliveira Sousaa, Paula Rezende Camargo
a*, Ivana Leão Ribeiro
a, Rodrigo Bezerra de Menezes 4
Reiffb, Lori Ann Michener
c, Tania Fátima Salvini
a 5
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aDepartment of Physical Therapy, Federal University of São Carlos, São Carlos, SP, Brazil 7
bDepartment of Medicine, Federal University of São Carlos, São Carlos, SP, Brazil 8
cDepartment of Physical Therapy, Virginia Commonwealth University, Richmond, VA, USA 9
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* Corresponding author 11
Paula Rezende Camargo 12
Departamento de Fisioterapia 13
Universidade Federal de São Carlos 14
Rodovia Washington Luis, km 235, CEP: 13565-905, São Carlos, SP, Brasil. 15
E-mail address: [email protected] 16
Telephone: 55 16 3306 6696 17
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Keywords: shoulder pain; movement; biomechanics 19
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Abstract 1
This study described the three-dimensional shoulder motion during the arm elevation in individuals with isolated 2
acromioclavicular osteoarthritis (ACO) and ACO associated with rotator cuff disease (RCD), as compared to 3
controls. Seventy-four participants (ACO=23, ACO+RCD=25, Controls=26) took part of this study. Disability was 4
assessed with the DASH, three-dimensional kinematics was collected during arm elevation in the sagittal and 5
scapular planes, and pain was assessed with the 11-point numeric pain rating scale. For each kinematic variable 6
and demographic variables, separate linear mixed-model 2-way ANOVAs were performed to compare groups. 7
Both ACO groups had higher DASH and pain scores. At the scapulothoracic joint, the isolated ACO group had 8
greater internal rotation than control, and the ACO+RCD group had greater upward rotation than both other 9
groups. At the sternoclavicular joint, both groups with ACO had less retraction, and the isolated ACO group had 10
less elevation and posterior rotation. At the acromioclavicular joint, the isolated ACO group had greater upward 11
rotation, and both ACO groups had greater posterior tilting. Patients with ACO had altered shoulder kinematics, 12
which may represent compensatory responses to reduce pain and facilitate arm motion during arm elevation and 13
lowering. 14
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Keywords: shoulder pain; movement; biomechanics 16
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Introduction 1
Acromioclavicular (AC) joint pathology can cause shoulder pain. Cartilaginous degeneration can occur 2
from the high axial loads transferred through the small and incongruent joint surface area during complex 3
torsional movements during shoulder movements, leading to osteoarthritis[Babatunde et al., 2012; Buttaci et al., 4
2004]. Acromioclavicular osteoarthritis (ACO) can occur in isolation, but it is often associated with rotator cuff 5
disease (RCD)[Chen et al., 2003] due to the direct contact of the AC joint with the subacromial bursa and rotator 6
cuff tendons. Altered shoulder kinematics in those with ACO, with or without concurrent RCD, may be 7
compensatory or a contributing factor leading to shoulder pain and functional loss. 8
Altered scapulothoracic(ST) and sternoclavicular(SC) kinematics during active arm elevation have been 9
shown in those with RCD[Timmons et al. 2012]. Motion of the AC joint has only been described in asymptomatic 10
individuals during arm elevation from rest to 90°[Teece et al. 2008; Ludewig et al. 2009]. Shoulder kinematics 11
have not been evaluated in individuals with isolated ACO, or ACO associated with RCD. Characterizing the 12
pattern of kinematics alterations will elucidate the kinematic impairments that may be leading to or a 13
compensation for the presence of ACO. Furthermore, identifying the kinematic impairments can provide a 14
foundation for the selection of treatment interventions to address the deficits. Characterization of the 15
abnormalities in shoulder kinematics is clinically relevant for evaluation and treatment of ACO in those individuals 16
with or without RCD. 17
This study examined the three-dimensional shoulder motion during the ascending and descending 18
phases of arm elevation in individuals with isolated ACO and in those with RCD(ACO+RCD) as compared to 19
asymptomatic individuals in two planes of elevation (sagittal and scapular). We hypothesized that both ACO 20
groups would show kinematic deviations as compared to the asymptomatic group. Additionally, we hypothesized 21
individuals with ACO+RCD would have greater kinematic deviations than those with ACO only. This study is 22
presented in two parts. In part 1, we describe the three-dimensional shoulder motion at the ST, SC, and AC joints. 23
Part 2 reports shoulder muscle activity of the upper and lower trapezius, serratus anterior and anterior deltoid. 24
25
Methods 26
Participants 27
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Individuals (n=146) with shoulder pain between 18 and 60 years old, body mass index below 28 kg/m2, 1
greater than 6 months of pain without any physical intervention for the upper limb, and who were seeking physical 2
therapy treatment were screened for eligibility. A physical therapist with 7 years’ experience performed the initial 3
screening. Participants were included if they presented with 1- a history of shoulder pain greater than 1 week, 2- 4
localized pain at the top of the shoulder near or at the AC joint, or at the proximal anterolateral shoulder region or 5
deltoid area, and 3- at least one of the following signs: a- painful arc in a range of 90º to 180º, b- visual inspection 6
for deformity, swelling, erythema, or muscle wasting, c- palpable tenderness, pain, deformity or crepitus at the AC 7
joint, or d- positive cross-body adduction test[Buttaci et al., 2004; Buchberger 1999;Babatunde et al. 2012]. If any 8
of the following were present, the participant was excluded: less than 120° of humeral elevation range of motion, 9
cervical spine–related symptoms; history of glenohumeral dislocation or instability, as determined by positive 10
apprehension, anterior drawer, or sulcus test; previous shoulder surgery; signs of a complete rotator cuff tear; 11
adhesive capsulitis; calcific tendinitis; previous clavicle, scapula or humerus fracture; neurologic and systemic 12
pathologies, and source of shoulder pain due to active trigger point located in upper trapezius. 13
After initial screening, participants had Zanca view radiographs and ultrasonography examinations 14
performed by a physician with expertise in musculoskeletal radiology. The radiographic signs for AC joint 15
degeneration were osteophytes, diminished joint space, sclerosis, erosion, and incongruence of the AC joint[van 16
Riet and Bell 2011]. The ultrasonography criteria for RCD diagnosis were fluid within the synovial sheath, tendon 17
hypoechogenicity, thickening, and thinning, or tendon fiber discontinuity[Naredo et al. 2002], and hypoechoic fluid 18
greater than 2mm thick on subacromial/subdeltoid bursa[Kelly et al. 2010]. 19
After screening, 48 patients qualified for kinematic measurements (Figure 1). According to the imaging 20
findings, 23 individuals were diagnosed with isolated osteoarthritis(ACO group); and 25 individuals with ACO and 21
RCD(ACO+RCD group). A cohort of asymptomatic individuals without shoulder pain (n=26) were matched to the 22
ACO groups for gender, age (+/-5 years), and BMI (+/-2). The control group was confirmed to not have any of the 23
inclusion and exclusion criteria as described prior. Thus, a total of 74 participants took part of the study (Table 1). 24
All participants gave their written informed consent to participate in this study, which was approved by the Ethical 25
Committee of the Federal University of São Carlos and conducted according to the Helsinki Statement. 26
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Insert Figure 1 about here 28
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1
Insert Table 1 about here 2
Procedures 3
Participants were first screened for inclusion and exclusion criteria, and then completed questions 4
regarding shoulder pain and demographics. Disability was assessed with the Brazilian version of the Disabilities 5
of the Arm, Shoulder and Hand (DASH) questionnaire[Orfale et al. 2005], with score range 0 to 100 (0=no 6
disability). Three-dimensional shoulder kinematics were collected during arm elevation (ascending and 7
descending phases) in the sagittal and scapular planes. The order of the plane to be evaluated was randomly 8
chosen. The symptomatic shoulder was evaluated in subjects with ACO, and the shoulder for the asymptomatic 9
healthy subjects was randomly chosen. 10
11
Three-dimensional kinematics 12
Three-dimensional motion data were collected using the Flock of Birds electromagnetic tracking 13
system(Ascension Technologies, Burlington, VT) and Motion Monitor software(Innovative Sports Training, 14
Chicago, IL) using an 16-bit A/D conversion. The root mean square (RMS) accuracy of the electromagnetic 15
system is 0.5° for orientation and 0.18cm for position, as reported by the manufacturer. Sensors were placed on 16
the 3 body segments of the clavicle, scapula, humerus, and thoracic. The transmitter defined the global reference 17
frame. The sampling rate for each sensor was 100Hz. 18
Individuals stood in a neutral position with the transmitter behind the tested shoulder. Three surface 19
electromagnetic sensors were attached to the skin using double-sided tape on the sternum, on the lateral third of 20
the clavicle, on flat surface on the posterior acromion process, and to the humerus via a cuff secured with Velcro 21
right above the humeral epicondyles. One of the sensors attached to a stylus was used to digitize anatomical 22
landmarks to create local anatomical coordinate systems for each rigid segment. Anatomical coordinate systems 23
were established for each segment as per the International Society of Biomechanics protocol[Wu et al. 2005]. 24
Next, participants were instructed to perform 3 repetitions of elevation and lowering in the sagittal plane 25
(90° of humerothoracic angle) and the scapular plane (40° anterior to the frontal plane). To maintain the plane of 26
elevation, participants were instructed to lightly contact their fingertip on the vertical planar surface and with the 27
thumb pointed superiorly during active elevation (Figure 2). Participants were given verbal cues to control the 28
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speed of motion (3 seconds up and 3 seconds down) for 3 repetitions. This procedure has been shown to have 1
high trial-to-trial within day reliability during elevation and lowering of the arm in asymptomatic subjects and 2
subjects with rotator cuff disease[Haik et al, 2014]. Individuals self-reported their pain during arm elevation by the 3
numeric pain rating scale(NPRS; 0-10, 0=no pain and 10=the worst pain imaginable)[Puga et al. 2013]. 4
5
Insert Figure 2 about here 6
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Data reduction 8
The local coordinate systems of the sensors were transformed to clinically meaningful axis systems 9
based on the digitized anatomical landmarks, with orthogonal system of the z-axis pointed laterally, the x-axis 10
pointed anteriorly and y-axis superiorly for the shoulder[Wu et al. 2005]. The axis systems for trunk, scapula, 11
clavicle, and humerus were established as previously described[Ludewig et al. 2009]. To describe AC joint 12
motion, scapular axes were described relative to clavicular axes[Ludewig et al., 2009;Teece et al., 2008]. The 13
sequence Y-X-Z was used to describe scapular movements relative to the trunk, with the order: internal/external 14
rotation, upward/downward rotation and anterior/posterior tilting. The humerus relative to the trunk was 15
determined using the sequence Y-X'-Y ", with the first rotation defined the elevation plane, the second defined the 16
angle of humeral elevation, and the third defined the internal rotation/external[Wu et al. 2005]. Motion of the 17
clavicle relative to the sternum was defined as protraction/retraction about the superior axis, elevation/depression 18
about the anterior axis, and anterior/posterior rotation about the lateral axis. Motion of the scapula relative to the 19
clavicle was defined with use of the same terminology as for the scapula relative to the thorax[Ludewig et al. 20
2009]. Using the right-hand rule, positive motions were: scapular and AC downward rotation, internal rotation, and 21
posterior tilting; clavicular depression, posterior rotation, and retraction. Angular values for ST motions were 22
extracted at rest, at 30°, 60°, 90°, and 120° of humeral elevation; and for SC and AC motions, at rest, at 30°, 60°, 23
and 90° of humeral elevation during ascending and descending phases. 24
25
Data analysis 26
Means and standard deviations were calculated for all demographic and dependent variables. A Kruskal-27
Wallis test was conducted for gender and affected/tested limb. A one-way analysis of variance (ANOVA) was 28
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conducted to compare groups for age, height, mass, BMI, DASH, NPRS (for each plane) and each kinematic 1
variable in the rest position, using Tukey post-hoc test when applicable. For each kinematic variable, a separate 2
linear mixed-model 2-way ANOVA was performed for phase (ascending and descending) and plane, using 3
humeral elevation as the repeated factor and groups as the main factor. Comparisons of interest were the main 4
effect or interactions of group by humeral elevation. Comparisons between planes of motions were not made, as 5
this was not a hypothesis. The repeated covariance type was determined by Akaike's information criterion (AIC) 6
that is an index of model goodness-of-fit and may be used to compare models with the same fixed effects but 7
different covariance structures[Littell et al., 2000]. An alpha level of 0.05 was used for all statistical tests, and 8
post-hoc pairwise comparisons were made with a Bonferroni-adjusted alpha. Finally, inter-group effect sizes for 9
all comparisons for all variables were calculated using Cohen’s d coefficient[Cohen 1988]. An effect size > 0.8 10
was considered large, 0.5 moderate, and less than 0.2 small[Cohen 1988]. 11
12
Results 13
Participant characteristics, DASH and NPRS scores by group are presented in Table 1. No difference was 14
found between groups for any of the demographic variables. Groups with isolated ACO and ACO+RCD had 15
higher DASH and NPRS scores than the control group. Rest position for each kinematic variable is presented in 16
Tables 2, 3 and 4; and only between group differences found was for SC protraction/retraction (Table 3) in which 17
isolated ACO group had less SC retraction than the control group (mean difference=5.0°; p=0.03). 18
19
Insert Table 2 about here 20
21
Scapulothoracic(ST) Joint Motion 22
Figure 3–A shows the kinematic pattern of ST joint during the arm elevation; mean and standard 23
deviation in Table 2. 24
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Insert Figure 3 about here 26
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Sagittal plane. During the ascending phase, there was interaction (group X humeral elevation) for 1
internal/external rotation (p=0.04) and upward/downward rotation (p<0.01). Pairwise comparisons indicated the 2
individuals with isolated ACO had greater internal rotation compared to controls(mean difference=3.47°; effect 3
size=0.81) at 30° of arm elevation; and individuals with ACO+RCD had greater upward rotation compared to 4
controls(mean difference=5.25°; effect size=0.91) at 90° of arm elevation; and those with isolated ACO and 5
ACO+RCD had greater upward rotation compared to controls(mean differences=3.69° and 5.25°; effect 6
sizes=0.54 and 0.81, respectively) at 120° of arm elevation. During the descending phase, there was an 7
interaction (group X humeral elevation) for internal/external rotation (p=0.01) and upward/downward rotation 8
(p=0.01); with pairwise comparisons indicating that individuals with ACO+RCD had increased upward rotation 9
compared to controls(mean difference=3.69°; effect size=0.67) at 90° of elevation; individuals with ACO+RCD 10
had increased internal rotation(mean difference=4.44°; effect size=0.80); and upward rotation(mean 11
difference=3.66°; effect size=0.57) compared to controls at 120° of elevation. 12
Scapular plane. During the ascending phase, there was a main effect of group for internal/external 13
rotation(p=0.02) and upward/downward rotation(p<0.01), in which individuals with isolated ACO presented 14
increased internal rotation compared to controls(mean difference=2.43°; effect size=0.34) and individuals with 15
ACO+RCD presented increased upward rotation compared to individuals with isolated ACO and controls(mean 16
differences=2.49° and 3.65°; effect sizes=0.18 and 0.29, respectively). During the descending phase, there was a 17
main effect of group for internal/external rotation(p<0.01) and upward/downward rotation(p<0.01), which 18
individuals with isolated ACO presented increased internal rotation compared to individuals with ACO+RCD(mean 19
difference=3.35°; effect size=0.53) and individuals with ACO+RCD presented increased upward rotation 20
compared to individuals with isolated ACO and controls(mean differences=2.09° and 2.94; effect sizes=0.16 and 21
0.24, respectively). No differences were found for ST anterior/posterior tilting in either plane. 22
23
Sternoclavicular(SC) Joint Motion 24
Figure 3–B shows the kinematic pattern of SC joint during the arm elevation; mean and standard 25
deviations in Table 3. 26
Sagittal plane. During the ascending phase, there were group differences for retraction/protraction 27
(p<0.01) and anterior/posterior rotation(p<0.01), which individuals with isolated ACO and ACO+RCD presented 28
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decreased retraction compared to controls(mean differences=4.48° and 3.38°; effect sizes=0.81 and 0.69, 1
respectively) and individuals with isolated ACO presented lesser posterior rotation than individuals with 2
ACO+RCD and controls(mean differences=6.97° and 4.74°; effect sizes=0.64 and 0.47, respectively). During the 3
descending phase, there was interaction (groups X humeral elevation) for retraction/protraction (p=0.02), and 4
pairwise comparisons indicated that individuals with isolated ACO and ACO+RCD had lesser retraction than 5
controls(mean differences=4.98° and 4.17°; effect sizes=1.08 and 0.81, respectively) at 30° of arm elevation. 6
There was a main effect for group for anterior/posterior rotation(p<0.01), and post-hoc tests indicated individuals 7
with isolated ACO had decreased posterior rotation than ACO+RCD and controls(mean differences=6.34° and 8
4.14°; effect sizes=0.61 and 0.42, respectively). No differences were found for SC elevation/depression. 9
Scapular plane. During the ascending phase, there was a main effect of group for elevation/depression 10
(p<0.01) and anterior/posterior rotation(p=0.02). Post-hoc tests indicated individuals with isolated ACO had 11
decreased elevation as compared to ACO+RCD and controls(mean differences=3.26° and 2.24°; effect 12
sizes=0.67 and 0.42, respectively), and decreased posterior rotation as compared to individuals with 13
ACO+RCD(mean difference=2.99°; effect size=0.34). During the descending phase, there was a main effect of 14
group for elevation/depression(p=0.01) and anterior/posterior rotation(p=0.03); post-hoc testing indicating those 15
with isolated ACO had less elevation than ACO+RCD and controls(mean differences=2.21° and 2.64°; effect 16
sizes=0.39 and 0.46, respectively) and less posterior rotation compared to individuals with ACO+RCD and 17
controls(mean differences=3.57° and 3.53°; effect sizes=0.36 and 0.38, respectively). No differences were 18
detected for SC retraction/protraction in either plane of motion. 19
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Insert Table 3 about here 21
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Acromioclavicular(AC) Joint Motion 23
Figure 3–C shows the kinematic pattern of AC joint during the arm elevation; mean and standard 24
deviations in Table 4. 25
Sagittal plane. During the ascending phase, there was a main effect for group for upward/downward 26
rotation(p<0.01) which individuals with isolated ACO presented increased upward rotation compared to individuals 27
with ACO+RCD and controls(mean differences=4.06° and 3.18°; effect sizes=0.65 and 0.61, respectively). There 28
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was interaction (groups X humeral elevation) for anterior/posterior tilting(p=0.02), and pairwise comparisons 1
indicated that, individuals with isolated ACO had increased posterior tilt compared to controls(mean 2
difference=6.83°; effect size=0.82) in 60° of elevation, and those with isolated ACO and ACO+RCD had increased 3
posterior tilt as compared to controls in 90° of elevation (mean differences=6.62° and 5.30°; effect sizes=0.94 and 4
0.68, respectively). During the descending phase, there was a group main effect for upward/downward 5
rotation(p=0.02) which individuals with isolated ACO presented increased upward rotation compared to 6
controls(mean difference=4.27°; effect size=0.82). No differences were found for AC anterior/posterior tilting. 7
Scapular plane. During the ascending phase, there was interaction (group X humeral elevation) for 8
upward/downward rotation(p=0.02), and pairwise comparisons indicated individuals with isolated ACO had 9
increased upward rotation as compared to ACO+RCD and controls in 90° of elevation(mean differences=4.61° 10
and 6.57°; effect sizes=0.74 and 1.55, respectively). During the descending phase, there was interaction (group X 11
humeral elevation) for upward/downward rotation(p=0.04), which pairwise comparisons indicated that individuals 12
with isolated ACO and ACO+RCD had increased upward rotation compared to controls in 90° of elevation(mean 13
differences=8.08° and 5.73°; effect sizes=0.85 and 0.53, respectively). No differences were found for AC 14
internal/external rotation in either plane of motion. 15
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Insert Table 4 about here 17
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Discussion 19
To our knowledge, this is the first study to characterize the motion of ST, SC and AC joints in the shoulder 20
complex in individuals with isolated ACO and ACO+RCD. These individuals have alterations in kinematics during 21
arm elevation in both ascending and descending phases in both the sagittal and scapular planes of motion. 22
Specifically, individuals with isolated ACO had more ST internal rotation than controls, and those with ACO+RCD 23
had more ST upward rotation than both the isolated ACO and control groups in both planes of arm elevation. At 24
the SC joint, both groups with ACO had less retraction in sagittal plane, and the group with isolated ACO had less 25
elevation in the scapular plane and posterior rotation in both planes as compared to other two groups. For the AC 26
joint, the group with isolated ACO presented with more AC upward rotation in both planes, and both groups with 27
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ACO had more AC posterior tilt in sagittal plane than the control group. These alterations may be due to the 1
disease pathology of ACO and RCD, or serve as compensatory responses to reduce pain and elevate the arm. 2
Generally, our data agree with previous studies[Ludewig et al., 2009; Ludewig et al., 2010; McClure et al., 3
2006; Teece et al., 2008] with respect to the pattern and amount of motion for the analyzed joint motions. For the 4
ST motion, we found kinematic deviations in those with ACO of increased scapular internal rotation. There was 5
generally more ST internal rotation in those with ACO disease. During ascending phase, participants with isolated 6
ACO had increased internal rotation as compared with controls in both planes. However, in the sagittal plane, 7
increased internal rotation occurred only at 30° of arm elevation, which may in part be explained by the slightly 8
greater (non-significant) internal rotation of 2.1° in the rest position in those with isolated ACO. Greater internal 9
rotation can be a causative factor of greater AC joint compression, contributing to degeneration and joint pain. 10
Increased ST internal rotation has been shown to be related to a short pectoralis minor muscle[Borstad et al., 11
2005), however we did not measure pectoralis minor length. Conversely, there was decreased ST internal rotation 12
during the descending phase in participants with ACO+RCD compared to controls and isolated ACO groups. This 13
decreased ST internal rotation in participants with ACO+RCD occurred in the high levels of arm elevation, where 14
participants with RCD often report painful movement, especially during the descending phase [Borstad et al., 15
2002]. Thus, decreased ST internal rotation in participants with ACO+RCD can be one strategy to avoid the pain 16
in the highest level of arm elevation, or this alteration may be related to the greater ST upward rotation seen. 17
At the ST joint, we also found changes in scapular upward rotation. Interestingly, we found a main effect 18
of increased upward rotation in those with ACO+RCD as compared to both controls and those with isolated ACO. 19
This increased upward rotation reported prior in those with RCD may be due to an attempt to decease rotator cuff 20
compression in the subacromial space or tendon load[Timmons et al. 2012]. Prior literature has shown that the 21
greatest amount of pain is present at the higher arm elevation angles in those with AC joint dysfunction 22
[Babatunde et al. 2012; Buttaci et al. 2004; Chen et al. 2003]. However, they also commonly report pain during 23
the entire range of arm elevation and potentially even at rest. Our patients generally reported pain across the 24
range of motion, not just at end range of arm elevation. This likely partially explains why those with ACO (isolated 25
and with RCD) had kinematic deviations at across the arm elevation angles (both lower and higher angles). 26
At the SC joint, the general pattern of motion found in our study was similar to a prior findings[Ludewig et 27
al. 2004]. Our results suggest there are differences between planes of elevation, evidenced by SC 28
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retraction/protraction and elevation/depression motions. For SC retraction/protraction, in sagittal plane during both 1
phases of motion, participants with ACO had less retraction than controls. For SC elevation/depression, there was 2
no difference between groups in sagittal plane, but our results showed that, in scapular plane, participants with 3
isolated ACO presented less elevation than other participants during the both phases of the motion. 4
Reduced SC retraction may be related to the finding of greater ST internal rotation found in participants 5
with isolated ACO, especially in the lower levels of arm elevation and during the descending phase of the motion. 6
It is important to note that participants with isolated ACO presented in the rest position with less SC retraction as 7
compared to controls (mean difference=3.30°). Participants with ACO+RCD also presented less SC retraction, 8
which is related to the greater ST upward rotation that occurred in two planes, and also related to greater SC 9
elevation in scapular plane. For SC anterior/posterior rotation, there was no difference between planes or phases, 10
and participants with isolated OAC showed less posterior rotation than participants with ACO+RCD and controls. 11
The lesser posterior rotation in participants with isolated ACO can be related with the greater ST internal rotation. 12
When we analyzed the AC joint motion, participants with isolated ACO presented greater AC upward 13
rotation than the other two groups (even participants with ACO+RCD–during ascending phase) in the sagittal 14
plane. We also found that both groups with ACO had greater posterior tilt during ascending arm elevation. On the 15
other side, in scapular plane, both groups with ACO presented with greater AC upward rotation than the controls 16
in the highest of the arm elevation (90°) and no difference for AC tilting. This greater AC upward rotation and 17
posterior tilt in the groups with ACO, can be characterized by greater movement of the AC joint and thought as 18
one of the causes of the osteoarthritis. However, the participants with ACO+RCD may have created another 19
strategy to avoid pain because of the addition of RCD pathology, as they presented with decreased AC upward 20
rotation. Opposite from our findings for the ST joint, we did not find differences with AC internal/external rotation 21
between groups, which can be occurred due compensations in other motions and joints. 22
This study has an important clinical relevance for rehabilitation, by providing enhanced understanding of 23
the motion of AC, SC, and ST joints of the shoulder complex in conditions of ACO and ACO associated with RCD. 24
Individuals with isolated ACO presented with more kinematics deviations than individuals with ACO+RCD, when 25
compared to controls at the ST, SC, and AC joints. The literature has shown that individuals with RCD have more 26
ST internal rotation and less ST upward rotation, and increased SC elevation and retraction[Timmons et al. 2012] 27
as compared to controls. In the current study, those with RCD (ACO+RCD) had increased ST upward rotation and 28
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decreased SC retraction. Those with isolated ACO additionally had less SC elevation and posterior rotation as 1
compared to those with ACO+RCD and controls. At the AC joint, individuals with ACO had increased AC upward 2
rotation as compared to the other groups. Those with isolated ACO had more kinematic deviations than those 3
with the coexistence of RCD. The presence of RCD appears to mitigate the kinematic alterations of ACO. 4
Rehabilitation techniques that aim to restore these kinematic impairments may serve to reduce pain and 5
improve disability. Exercises that involve cross-body adduction should be avoided, since this increases scapular 6
internal rotation relative to the clavicle[Ludewig et al. 2009]. Movements and motor control strategies that 7
emphasize scapular external rotation may be beneficial. Excessive upward rotation may represent a 8
compensatory response for glenohumeral weakness or glenohumeral joint stiffness or an attempt to reduce direct 9
subacromial impingement in those with ACO+RCD. Strengthening and motor control exercises to reduce 10
excessive upward rotation may be beneficial to reduce pain and improve shoulder function. Excess SC elevation 11
and retraction can be associated to excess upper trapezius activation[Phadke et al. 2009], and therefore 12
stretching or relaxation techniques for the upper trapezius may be effective. 13
This study presents some limitations. We evaluated a broad range of age of individuals which may have 14
increased the variability of the data. This study identified statistical and clinically meaningful differences in 15
shoulder kinematics. Differences of ~ 5o for ST upward/downward rotation[McClure et al. 2006], and for clavicular 16
motions[Roy et al. 2010] were considered clinically meaningful based on prior studies of differences in kinematics 17
between those with and without shoulder pain. Also, moderate to large effect sizes were demonstrated for 18
majority of the statistical differences. We did not propose to investigate differences between planes of arm 19
elevation, because the main objective was to characterize the joint motions for those with and without ACO. 20
21
Conclusions 22
Individuals with ACO, both isolated and associated to RCD, had increased ST upward rotation, less SC 23
retraction and greater AC posterior tilt than controls. Also, individuals with isolated ACO had some more 24
alterations, such as increased ST internal rotation, less SC elevation and posterior rotation, and greater AC 25
upward rotation and posterior tilt than controls. These alterations may represent compensatory responses as an 26
attempt to reduce pain. Alternatively, the kinematics alterations may be the cause of their shoulder pain and 27
disability. Nevertheless, we also found some differences between individuals with isolated ACO and ACO+RCD 28
Page 15
14
that seem be related to plane of motion, as well as, due to coexisting pathologic conditions that can exacerbate 1
the kinematics deviations. More work is necessary to clarify these alterations. 2
3
4
Conflicts of Interest 5
There are no conflicts of interest. 6
Acknowledgments 7
All the authors acknowledge the participants for their contribution. 8
Funding Source 9
C. O. Sousa is grateful to CNPq (Process #141309/2011-3) and FAPESP (Process # 2011/14642-9) for her 10
doctoral scholarships. 11
12
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18
19
Figure captions 20
21
Figure 1. Flow diagram of the participants with shoulder pain. 22
23
Figure 2. Participant setup with electromagnetic sensors and EMG surface sensors, in place: A) initial position, 24
B) during the movement. 25
26
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Figure 3. Mean and standard error of kinematic variables of A) Scapulothoracic joint; B) Sternoclavicular joint; 1
and C) Acromioclavicular joint, in degrees, during ascending and descending phases of humerothoracic elevation 2
in sagittal and scapular planes. 3
4
Page 22
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Table 1. Characteristics of all participants. 1
Characteristic Isolated ACO (n=23) ACO+RCD (n=25) Control (n=26) Test and P values
Age (y) 42.78±11.74 48.16±8.69 45.81±8.68 F=2.58;P=0.08
Gender 15 M; 8 F 13 M; 12 F 13 M; 13 F H=1.30; P=0.52
Height (m) 1.72±1.2 16.6±1.0 16.6±0.8 F=3.24; P=0.05
Mass (kg) 75.21±14.17 70.18±9.67 66.27±9.32 F=3.97; P=0.24
BMI (kg/m2) 25.05±2.17 25.28±2.36 24.10±2.49 F=1.82; P=0.17
Affected/Tested limb 11D; 12ND 18 D; 7 ND 17 D; 9 ND H=3.11; P=0.21
DASH, Mean (SD) 31.62 (21.09)a 38.59 (16.07)
b 1.02 (2.10)
a,b F=44.86; P<0.01
NPRS, Mean (SD), range
Sagittal plane
2.58(2.71), 0.00 – 8.00a
3.79(2.49), 0.00 – 8.00
b
0.00(0.00), 0.00 – 0.00a,b
F=21.91; P<0.01
Scapular plane 2.69(2.82), 0.00 – 8.33a 2.69(2.37), 0.00 –
8.50b
0.00(0.00), 0.00 – 0.00a,b
F=13.98;P<0.01
2
Note: M = male; F = female; D = dominant; ND = non-dominant. F = ANOVA test, H = Kruskal-Wallis test 3
a = difference between Isolated ACO and control groups. 4
b = difference between ACO+RCD and control groups. 5
6
7
8
Page 23
1
Table 2. Scapulothoracic (ST) Internal/External Rotation (IR/ER), Upward/Downward Rotation (UR/DR) and Anterior/Posterior Tilting (in degrees) during
ascending and descending phases of arm elevation in sagittal and scapular planes of motion in three groups (ACO, ACO+RCD, and Control).
Sagittal plane Scapular plane
Arm elevation angle
Ascending phase
F=2.2,p=0.04
Descending phase
F=2.8,p=0.01
Ascending phase
F=4.3,p=0.02
Descending phase
F=6.9,p<0.01
IR/ER
ACO ACO+RCD Control ACO ACO+RCD Control ACOa ACO+RCD Control
a ACO
b ACO+RCD
b Control
Rest
F=1.3,p=0.3
29.64 (3.75)
28.96 (5.77)
27.47 (4.58)
30° 39.07 (5.07)
a
37.69 (4.09)
35.64 (3.51)
a
40.59 (6.27)
38.21 (5.04)
37.41 (4.09)
32.53 (5.78)
31.42 (4.70)
29.75 (5.35)
32.30 (6.41)
30.45 (5.28)
30.07 (4.96)
60° 42.60 (5.80)
41.01 (4.26)
39.64 (3.58)
43.46 (6.76)
40.38 (5.14)
40.30 (5.04)
34.00 (6.04)
31.87 (4.76)
31.45 (5.09)
32.88 (6.56)
30.31 (5.21)
30.62 (4.18)
90° 4.44 (6.89)
43.20 (5.06)
40.70 (4.07)
43.25 (6.83)
41.04 (4.48)
41.43 (5.42)
34.74 (7.39)
31.61 (4.78)
32.14 (4.68)
32.75 (7.80)
29.19 (4.89)
30.74 (4.61)
120° 42.12 (6.96)
40.12 (5.35)
41.62 (5.41)
39.85 (7.57)
35.86 (5.69)
c
40.83 (5.06)
c
32.51 (9.02)
30.92 (4.47)
30.73 (7.42)
32.62 (9.46)
27.21 (5.18)
30.66 (7.43)
Arm elevation angle
Ascending phase
F=3.9,p<0.01
Descending phase
F=3.0,p=0.01
Ascending phase
F=11.7,p<0.01
Descending phase
F=7.7,p<0.01
UR/DR ACO ACO+RCD Control ACO ACO+RCD Control ACOb ACO+RCD
b,c Control
c ACO
b ACO+RCD
b,c Control
c
Rest
F=2.3,p=0.1
-1.26 (4.35)
-3.93 (4.37)
-3.03 (4.51)
30° -7.55 (4.70)
-9.94 (5.67)
-9.03 (4.42)
-8.77 (4.20)
-9.31
(6.61)
-10.29 (4.34)
-6.38 (4.64)
-9.55 (4.43)
-7.94 (4.89)
-7.30 (4.54)
-9.85 (5.50)
-9.21 (5.53)
60° -16.16 -19.15 -16.53 -16.43 -17.74 -17.33 -17.55 -21.18 -17.77 -16.63 -18.95 -17.14
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(6.22) (5.15) (4.59) (4.68) (7.39) (4.71) (5.22) (5.60) (5.03) (4.95) (5.97) (5.28)
90° -27.79 (7.59)
-31.13 (5.99)
c
-25.88 (5.53)
c
-30.02 (5.35)
-31.32 (6.35)
c
-27.67 (4.68)
c
-29.99 (5.99)
-32.13 (6.73)
-27.79 (4.82)
-29.05 (4.69)
-31.63 (5.99)
-27.24 (4.60)
120° -40.22 (7.39)
a
-41.53 (6.64)
c
-36.52 (6.33)
a,c
-41.48 (6.95)
-42.04 (6.64)
c
-38.35 (6.17)
c
-40.28 (5.80)
-41.31 (6.86)
-36.05 (4.61)
-40.25 (5.66)
-41.13 (6.63)
-36.23 (4.99)
Arm elevation angle
Ascending phase
F=1.0,p=0.4
Descending phase
F=0.4,p=0.7
Ascending phase
F=0.4,p=0.7
Descending phase
F=0.6,p=0.2
Tilting ACO ACO+RCD Control ACO ACO+RCD Control ACO ACO+RCD Control ACO ACO+RCD Control
Rest
F=0.5,p=0.6
-7.77 (4.80)
-8.78 (3.80)
-7.60 (4.49)
30° -2.29 (5.60)
-2.27 (3.76)
2.80 (2.97)
-0.80 (4.70)
-2.40 (3.67)
-1.18 (3.26)
-6.01 (5.36)
-5.42 (4.19)
-4.59 (3.16)
-5.31 (4.60)
-5.35 (4.36)
-4.01 (4.54)
60° 1.70 (6.29)
1.59 (3.60)
0.38 (3.17)
1.60 (5.61)
-0.12 (4.33)
1.20 (3.35)
-1.08 (5.38)
-0.58 (3.57)
-1.04 (4.08)
-1.96 (5.79)
-1.10 (3.66)
-0.39 (4.62)
90° 5.24 (7.79)
4.96 (3.71)
4.03 (4.36)
5.23 (7.72)
4.22 (4.87)
4.95 (4.58)
3.38 (6.19)
4.71 (4.11)
3.36 (4.70)
3.97 (7.02)
4.81 (3.69)
4.78 (4.96)
120° 9.45 (8.42)
10.70 (5.06)
9.19 (4.80)
10.14 (8.83)
11.64 (5.74)
9.96 (4.60)
9.14 (6.91)
10.85 (4.10)
9.75 (5.70)
9.24 (8.31)
12.02 (5.20)
10.96 (5.79)
Values are means and standard deviation (SD). a = difference between Isolated ACO and control groups; b = difference between Isolated ACO and
ACO+RCD groups; c = difference between ACO+RCD and control groups.
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Table 3. Sternoclavicular (SC) Retraction/Protraction (Ret/Prot), Elevation/Depression (Elev/Dep) and Anterior/Posterior Rotation (Rot), in degrees, during
ascending and descending phases of arm elevation in sagittal and scapular planes of motion in three groups (ACO, ACO+RCD, and Control).
Sagittal plane Scapular plane
Arm elevation angle
Ascending phase
F=6.6,p<0.01
Descending phase
F=3.0,p=0.02
Ascending phase
F=0.2,p=0.8
Descending phase
F=1.3,p=0.3
Ret/Prot ACOa ACO+RCD
c Control
a,c ACO ACO+RCD Control ACO ACO+RCD Control ACO ACO+RCD Control
Rest
F=3.8,p=0.03
-27.98 (7.68)
a
-31.28 (5.71)
-32.98 (5.75)
a
30° -21.55
(4.01)
-23.18
(3.40)
-26.76
(5.03)
-22.16
(4.51)a
-22.97
(5.57)c
-27.14
(4.71)a,c
-28.66
(5.46)
-29.29
(4.59)
-30.45
(5.08)
-28.96
(6.84)
-29.66
(6.93)
-31.15
(5.25)
60° -22.69
(4.85)
-24.03
(3.46)
-28.33
(4.82)
-22.31
(6.33)
-25.46
(6.86)
-28.41
(5.53)
-33.89
(5.42)
-34.01
(6.11)
-34.17
(5.42)
-33.04
(6.94)
-34.35
(7.83)
-34.74
(6.44)
90° -28.21
(6.93)
-29.38
(5.09)
-31.01
(4.03)
-31.97
(6.59)
-33.69
(7.75)
-32.55
(4.94)
-38.96
(5.97)
-39.14
(6.99)
-38.91
(6.35)
-39.30
(6.56)
-40.99
(7.05)
-40.88
(6.88)
Arm elevation angle
Ascending phase
F=0.5,p=0.6
Descending phase
F=0.3,p=0.7
Ascending phase
F=10.4,p<0.01
Descending phase
F=5.3,p=0.01
Elev/Dep ACO ACO+RCD Control ACO ACO+RCD Control ACOa,b
ACO+RCDb Control
a ACO
a,b ACO+RCD
b Control
a
Rest
F=0.4,p=0.7
-11.93 (5.24)
-12.25 (4.34)
-13.13 (5.10)
30° -16.33
(2.64)
-15.46
(5.28)
-16.59
(3.80)
-15.74
(6.07)
-16.04
(5.75)
-15.80
(4.13)
-12.94
(3.12)
-15.33
(3.06)
-15.52
(5.00)
-19.04
(5.34)
-14.15
(5.01)
-15.27
(4.96)
60° -18.78
(3.86)
-18.98
(4.27)
-18.32
(4.18)
-17.33
(6.78)
-18.45
(5.58)
-17.42
(4.90)
-17.91
(3.32)
-21.01
(2.74)
-19.32
(4.64)
-15.83
(5.41)
-17.92
(4.88)
-18.42
(5.07)
90° -21.47
(6.39)
-23.88
(5.11)
-21.12
(5.43)
-22.82
(8.39)
-22.26
(6.72)
-21.17
(5.67)
-20.42
(4.41)
-24.71
(3.03)
-23.16
(5.22)
-12.85
(4.90)
-22.28
(4.40)
-21.96
(5.22)
Arm elevation angle
Ascending phase
F=20.3,p<0.01
Descending phase
F=9.3,p<0.01
Ascending phase
F=4.1,p=0.02
Descending phase
F=3.8,p=0.03
Rot ACOa,b
ACO+RCDb Control
a ACO
a,b ACO+RCD
b Control
a ACO
b ACO+RCD
b Control ACO
a,b ACO+RCD
b Control
a
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2
Rest
F=0.3,p=0.8
-9.03 (12.93)
-6.68 (15.86)
-6.11 (15.61)
30° 15.44
(5.63)
21.00
(6.18)
19.35
(5.96)
17.90
(8.10)
24.76
(8.27)
23.17
(8.98)
15.44
(6.63)
21.00
(6.18)
19.35
(5.96)
6.68
(5.18)
8.48
(7.46)
9.97
(7.14)
60° 25.76
(5.65)
31.54
(5.93)
29.85
(6.87)
27.31
(6.33)
32.60
(8.40)
29.89
(8.57)
25.76
(5.65)
31.54
(5.93)
29.85
(6.87)
13.03
(5.89)
16.77
(8.86)
16.21
(8.08)
90° 32.24
(4.63)
44.81
(8.66)
41.45
(5.74)
33.20
(7.26)
40.06
(11.53)
37.78
(7.88)
35.24
(4.63)
44.81
(8.66)
41.45
(5.74)
19.90
(7.84)
25.06
(11.60)
24.01
(10.84)
Values are means (SD). a = difference between Isolated ACO and control groups; b = difference between Isolated ACO and ACO+RCD groups; c =
difference between ACO+RCD and control groups.
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Table 4. Acromioclavicular (AC) Internal/External Rotation (IR/ER), Upward/Downward Rotation (UR/DR) and Anterior/Posterior Tilting (in degrees) during
ascending and descending phases of arm elevation in sagittal and scapular planes of motion in three groups (ACO, ACO+RCD, and Control).
Sagittal plane Scapular plane
Arm elevation angle
Ascending phase
F=1.1,p=0.3
Descending phase
F=0.8,p=0.4
Ascending phase
F=0.3,p=0.7
Descending phase
F=0.08,p=0.9
IR/ER ACO ACO+RCD Control ACO ACO+RCD Control ACO ACO+RCD Control ACO ACO+RCD Control
Rest
F=0.2,p=0.8
58.90 (5.23)
58.32 (6.17)
59.49 (7.80)
30° 60.09
(4.87)
58.18
(8.00)
59.29
(6.72)
63.54
(5.65)
62.98
(8.06)
64.73
(8.92)
59.93
(4.89)
58.89
(5.86)
59.85
(6.70)
60.00
(5.78)
59.33
(7.13)
60.11
(7.65)
60° 63.00
(5.44)
60.00
(8.32)
61.17
(8.17)
63.00
(5.44)
60.00
(8.32)
61.17
(8.17)
63.09
(5.16)
60.56
(6.40)
61.99
(7.84)
62.07
(5.73)
60.80
(8.28)
61.53
(8.98)
90° 63.54
(5.65)
62.98
(8.06)
64.73
(8.92)
60.09
(4.87)
58.18
(8.00)
59.29
(6.72)
64.06
(5.92)
62.06
(7.27)
64.24
(9.47)
62.99
(6.77)
61.28
(7.34)
63.38
(10.07)
Arm elevation angle
Ascending phase
F=6.5,p<0.01
Descending phase
F=4.3,p=0.02
Ascending phase
F=3.2,p=0.02
Descending phase
F=2.6,p=0.04
UR/DR ACOa,b
ACO+RCDb Control
a ACO
a ACO+RCD Control
a ACO ACO+RCD Control ACO ACO+RCD Control
Rest
F=0.2,p=0.8
-3.55 (12.29)
-4.12 (13.28)
-1.67 (13.59)
30° 12.64
(4.51)
16.56
(7.02)
15.04
(5.11)
15.61
(6.24)
17.71
(8.99)
17.58
(7.53)
2.68
(4.48)
3.43
(7.97)
3.57
(4.00)
4.75
(5.32)
4.38
(8.64)
6.58
(6.00)
60° 13.14
(3.74)
16.77
(6.12)
15.27
(5.21)
15.53
(7.66)
15.52
(10.43)
18.73
(7.49)
-0.97
(4.28)
-0.20
(6.34)
1.01
(4.80)
2.75
(5.27)
1.18
(7.70)
5.67
(8.17)
90° 11.53
(6.43)
16.16
(9.52)
16.55
(6.36)
7.40
(7.85)
12.97
(7.98)
15.05
(8.46)
-5.82
(6.27)a,b
-1.21
(8.68)b
0.76
(8.22)a
-4.03
(8.04)a
-1.68
(10.70)c
4.06
(10.92)a,c
Arm elevation angle
Ascending phase
F=3.2,p=0.02
Descending phase
F=0.5,p=0.06
Ascending phase
F=2.3,p=0.1
Descending phase
F=0.5,p=0.6
Tilting ACO ACO+RCD Control ACO ACO+RCD Control ACO ACO+RCD Control ACO ACO+RCD Control
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2
Rest
F=0.1,p=0.9
6.44 (9.91)
6.66 (7.70)
7.30 (11.02)
30° 3.67
(6.22)
2.11
(7.74)
0.53
(7.87)
3.00
(8.35)
0.98
(9.51)
1.28
(7.97)
6.55
(5.01)
3.20
(5.17)
6.57
(4.79)
4.79
(4.35)
3.32
(7.03)
4.95
(6.35)
60° 7.50
(7.48)a
4.87
(9.46)
0.64
(9.07)a
6.41
(7.59)
1.99
(10.96)
2.00
(7.35)
13.36
(5.67)
10.27
(4.89)
11.47
(4.79)
8.54
(5.35)
7.20
(7.28)
8.98
(6.22)
90° 12.28
(9.25)a
10.96
(11.10)c
5.66
(9.66)a,c
11.54
(9.27)
12.35
(11.35)
9.77
(6.45)
19.27
(5.91)
16.22
(4.78)
17.74
(6.07)
17.13
(6.37)
15.25
(8.05)
16.67
(6.08)
Values are means (SD). a = difference between Isolated ACO and control groups; b = difference between Isolated ACO and ACO+RCD groups; c =
difference between ACO+RCD and control groups.
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1
2
3
4
5
6
Author Biography 7
8
Catarina de Oliveira Sousa received a B.Sc. in Physical Therapy (2005) from Federal University of Paraíba 9
(Brazil), a Master and a Ph.D. in Physical Therapy (2013) from Federal University of São Carlos (Brazil). She is 10
currently a professor at Federal University of Rio Grande do Norte (Brazil). Her research interests lie in defining 11
the biomechanical and neuromuscular impairments of the shoulder, and in the rehabilitation of these impairments 12
using movement training. 13
14
Paula Rezende Camargo received her bachelor’s degree, a Master and a PhD in Physical Therapy from 15
Universidade Federal de São Carlos (Brazil). She is currently Professor and Researcher in the Physical Therapy 16
Graduate Program at Universidade Federal de São Carlos (Brazil). Her research interests are shoulder 17
biomechanics and evidence-based rehabilitation for shoulder dysfunctions. 18
19
Ivana Ribeiro Leão received her bachelor’s degree in Physical Therapy from 20
Faculdade de Alagoas (Brazil). She received her Master from Federal University of São Carlos (Brazil), and is 21
currently a PhD student at Universidade Federal de São Carlos (Brazil). Her research interest is shoulder pain. 22
Rodrigo Bezerra de Menezes Reiff received his bachelor’s degree and PhD in Medicine in University of São 23
Paulo (Brazil) He is currently a Professor in Department of Medicine at Federal University of São Carlos (Brazil). 24
His research is focused on the evaluation and treatment of upper extremity orthopedic. 25
26
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Lori A. Michener, PhD, PT, ATC is currently a Professor and Director of the COOR (Clinical Orthopedic and 1
Sports Outcomes Research) Laboratory in the Department of Physical Therapy and joint appointments in the 2
Department of Physical Medicine and Rehabilitation and the Department of Anatomy and Neurobiology at Virginia 3
Commonwealth University, Richmond, VA. She earned a B.S. from Lock Haven University in PA, a B.S. in 4
Physical Therapy from the State University of New York at Buffalo, a MED from the University of Virginia, and 5
earned her PhD in Orthopedics and Biomechanics from MCP Hahnemann University in Philadelphia, PA. Her 6
research is focused on the understanding the mechanisms, diagnosis and treatment of upper extremity orthopedic 7
and sports injuries. 8
9
Tania Fátima Salvini is Physical Therapist and PhD in Physiological Science at University of São Paulo, Brazil. 10
She also underwent a training program in skeletal muscle plasticity at the Institute of Neurophysiology at 11
University of Bonn (Germany) and in the Neuromuscular Research Center at Boston University (USA). She is 12
currently Professor in the Department of Physical Therapy at Federal University of São Carlos, Brazil. Her 13
research interest is skeletal muscle plasticity and possible implications for physical therapy. 14
15
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Catarina de Oliveira Sousa 1
2
Paula Rezende Camargo 3
4
Ivana Leão ribeiro 5
6
Rodrigo Bezerra de Menezes Reiff 7
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1
Lori Ann Michener 2
3
Tania de Fátima Salvini 4
5
6