Ultrasonographic Measures of the Acromiohumeral Distance and Supraspinatus Tendon Thickness in Manual Wheelchair Users With Spinal Cord Injury

Accepted Manuscript Ultrasonographic measures of the acromiohumeral distance and supraspinatus tendon thickness in manual wheelchair users with spinal cord injury Amélie Fournier Belley, PT, Dany H. Gagnon, PT, PhD, François Routhier, PEng, PhD, Jean-Sébastien Roy, PT, PhD PII:

S0003-9993(16)30329-X

DOI:

10.1016/j.apmr.2016.06.018

Reference:

YAPMR 56606

To appear in:

ARCHIVES OF PHYSICAL MEDICINE AND REHABILITATION

Received Date: 10 May 2016 Accepted Date: 26 June 2016

Please cite this article as: Belley AF, Gagnon DH, Routhier F, Roy J-S, Ultrasonographic measures of the acromiohumeral distance and supraspinatus tendon thickness in manual wheelchair users with spinal cord injury, ARCHIVES OF PHYSICAL MEDICINE AND REHABILITATION (2016), doi: 10.1016/ j.apmr.2016.06.018. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

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Running Head: Shoulder ultrasound in wheelchair users

Ultrasonographic measures of the acromiohumeral distance and supraspinatus

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tendon thickness in manual wheelchair users with spinal cord injury

Amélie Fournier Belley, PT2; Dany H. Gagnon, PT, PhD3,4; François Routhier, PEng, PhD1,2; Jean-Sébastien Roy, PT, PhD1,2,¶

Department of Rehabilitation, Faculty of Medicine, Université Laval, Quebec City,

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Quebec, Canada, G1V 0A6

Centre for Interdisciplinary Research in Rehabilitation and Social Integration (CIRRIS),

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Institut de réadaptation en déficience physique de Québec (IRDPQ), Centre intégré universitaire de santé et de services sociaux de la Capitale-Nationale (CIUSSS-CN), Quebec City, Quebec, Canada, G1M 2S8

Centre de recherche interdisciplinaire en réadaptation (CRIR) du Montréal

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métropolitain, Institut de réadaptation Gingras-Lindsay-de-Montréal (IRGLM), Centre intégré universitaire de santé et de services sociaux de la Capitale-Nationale (CIUSSS-

School of Rehabilitation, Université de Montréal, Montreal (QC), Canada, H3C 3J7

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CN), Montreal, Quebec, Canada, H3S 1MG

Acknowledgments

This study was funded by the Ontario Neurotrauma Foundation (ONF) and the Réseau provincial de recherche en adaptation-réadaptation (REPAR- Quebec Rehabilitation Research Network). Dany Gagnon chairs the Initiative for the Development of New Technologies and Practices in Rehabilitation (INSPIRE) funded by the LRH Foundation.

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François Routhier holds a Junior 1 Research Career Award from the Fonds de la recherche en santé du Québec (FRQ-S). Jean-Sébastien Roy holds a Canadian Institute of

Conflicts of interest

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Health Research New Investigator Award and a FRQ-S Junior 1 Research Career Award.

The authors declared no conflicts of interest with respect to the authorship and/or publication of this article. Jean-Sébastien Roy, PT, PhD

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Corresponding Author:

Centre for Interdisciplinary Research in Rehabilitation and

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Social Integration, Institut de réadaptation en déficience physique de Québec (IRDPQ), Centre intégré universitaire de santé et de services sociaux de la Capitale-Nationale (CIUSSS-CN), 525, Boulevard Wilfrid-Hamel, Local H-

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1602, Québec (Qc), Canada, G1M 2S8. Telephone: (418) 529-9141 #6559; Fax: (418) 529-3548

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E-mail address: [email protected]

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Ultrasonographic measures of the acromiohumeral distance and supraspinatus

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tendon thickness in manual wheelchair users with spinal cord injury

3 Abstract

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Objective: 1) To evaluate the reliability of ultrasonographic (US) measures of

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acromiohumeral distance (AHD) in shoulder positions linked to wheelchair propulsion in

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manual wheelchair users (MWU) with spinal cord injury (SCI) and able-bodies; 2) to

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compare US measures of AHD, supraspinatus tendon thickness and occupation ratio

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between MWU with SCI with and without shoulder pain (rotator cuff [RC]

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tendinopathy); and 3) to compare these US measures between MWU with SCI and able-

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bodies.

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Design: Cross-sectional

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Setting: Two rehabilitation centers (Quebec City and Montreal)

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Participants: Objective 1: 16 MWU with SCI and 16 able-bodies; Objectives 2 and 3: 37

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MWU with SCI (17 with/20 without RC tendinopathy) and 26 able-bodies.

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Interventions: Not applicable.

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Main outcome measure: AHD and supraspinatus tendon thickness measured using US-

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imaging systems, as well as the occupation ratio of the supraspinatus tendon.

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Results: 1) Excellent intra- and interrater reliability of AHD was obtained in each arm

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position (ICC > 0.85); 2) MWU without shoulder pain have thicker tendon than MWU

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with RC tendinopathy; and 3) a significant Group x Position interaction was found for

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AHD measures when comparing MWU with SCI to able-bodies (greater AHD at the end

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of push phase for MWU with SCI). A thicker tendon and a higher occupation ratio were

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also found in MWU with SCI compared to able-bodies.

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Conclusion: US is a reliable technology to evaluate AHD in MWUs in shoulder

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positions linked to wheelchair propulsion. Supraspinatus tendon thickness and occupation

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ratio of AHD adequately discriminate between MWU with SCI and able-bodies. This

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shows that these US measurements can be used in future studies on SCI populations to

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better understand the changes at the shoulder joint in MWUs.

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Key Words: Ultrasonography; Shoulder; Wheelchairs; Spinal Cord Injury; Rotator Cuff;

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Pain.

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Preserving musculoskeletal integrity of the upper limbs remains essential among manual

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wheelchair users (MWU) with a spinal cord injury (SCI) since they rely greatly on their

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upper limbs to perform essential activities such as manual wheelchair propulsion and

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transfers.1 The performance of these activities, which are repeated many times throughout

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the day and require the generation of substantial and rapidly developing upper limb

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forces, expose the joints and soft tissues of the upper limbs to an increased risk of

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musculoskeletal impairment.2,3 In fact, the prevalence of full thickness rotator cuff (RC)

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tears is higher in MWU with SCI than in able-bodies matched for sex and age (63%

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compared with 15%).4 Therefore, shoulder pain is highly prevalent in MWU with SCI

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and is associated with lower subjective quality of life.4-7

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The acromiohumeral distance (AHD), considered a good indicator of the size of the

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subacromial space outlet, is defined as the smallest distance between the humeral head

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and inferior acromion.8 In able-bodies with RC tendinopathy, the dynamic narrowing of

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AHD during arm elevation is believed to play an important role in the aetiology of RC

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tendinopathy, and normalization of this dynamic variation is involved in the positive

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outcome of rehabilitation.9 The occupation ratio, which is defined as the supraspinatus

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tendon thickness expressed as a percentage of AHD, has been shown to be reduced in

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able-bodied individuals with RC tendinopathy,10 which could also explain the

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compression of the RC tendons during arm elevation. AHD, supraspinatus tendon

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thickness and occupation ratio have never been concomitantly evaluated in MWU with

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SCI. These measures could be used to evaluate MWU with SCI with RC tendinopathy to

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help in the choice of the treatment approach to promote and to monitor their effects over

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time.

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The first objective of this study was to determine the reliability of US measures of AHD

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in shoulder positions linked to wheelchair propulsion in able-bodied individuals and in

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MWU with SCI. The second objective was to compare AHD, supraspinatus tendon

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thickness and occupation ratio between MWU with SCI with and without RC disorders to

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better understand the factors that may explain the presence of shoulder pain in MWU

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with SCI. The third objective was, for the same variables, to compare MWU with SCI

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with and without RC tendinopathy to able-bodies to determine if MWU with SCI have

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different clinical characteristics.

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METHODS

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Population

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Three groups of participants (aged between 18 and 60 years) were recruited within a

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convenience sample: 1) MWU with SCI with RC tendinopathy, 2) MWU with SCI

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without RC tendinopathy and, 3) healthy able-bodied individuals. Inclusion criteria for

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MWU were: having SCI for more than six months and using manual wheelchair as the

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only means of locomotion for more than three months. MWU with RC tendinopathy also

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had, on the affected shoulder, one positive finding in each of the three following

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categories: 1) painful arc movement; 2) positive Neer test or Hawkins-Kennedy test; and

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3) pain on resisted isometric lateral rotation, abduction, or Jobe test.11

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For the three groups, exclusion criteria were: 1) previous shoulder surgery; 2) shoulder

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pain caused by neck pathology; or 3) shoulder capsulitis (restriction of passive

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glenohumeral movement of at least 30% for two or more directions).12 This study was

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approved by the Ethics Committee of the Institut de réadaptation en déficience physique

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de Québec and of the Centre de recherche interdisciplinaire en réadaptation (CRIR) du

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Montréal métropolitain.

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Study Design and experimental procedures:

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The study was divided in two parts (Part 1 – Reliability of US measures of AHD; Part 2 -

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Comparison of US measures between populations) and therefore included two cross-

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sectional studies with independent groups of subjects.

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Part 1 – Reliability of US measures of AHD

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Part 1 included one evaluation session during which US images of AHD were collected.

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US evaluations was performed with the participants seated in a manual wheelchair in five

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static upper limb positions (presented in the order in which they were evaluated; Figure

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1) 13: 1- arm at rest (0° of arm elevation with the hand pronated on the thigh), 2- at 45° of

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active shoulder abduction (ABD) with elbow at 90° of flexion, 3- beginning of the push

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phase (MIN); shoulder at 30° of extension, 4- position in which MWUs typically

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generate their peak torque during the push phase (PEAK); shoulder at 0° of flexion, and

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5- end of push phase (MAX); shoulder at 20° of flexion. The three positions linked to

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wheelchair propulsion were assessed while hands were positioned on the handrim and

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generating a 5 Nm total force (measured using SMARTWheel [Three River Holding,

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Mesa, Az]; a visual feedback of the force produced was given). All shoulder joint angles

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were measured with a goniometer and shoulder rotation was controlled to maintain a

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near-neutral position. The wheelchair was positioned on a platform used to lock the rear

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wheels with wooden blocks and the front wheels with a belt. A first evaluator collected

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three US images of AHD in each of the 5 positions. Then, a second evaluator repeated the

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same procedures (interrater reliability). Lastly, the first evaluator repeated the same

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procedures as initially performed (intrarater reliability). Each evaluator performed the

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calculation of the AHD blind after each image captured.

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Part 2 – Comparison of US measures of AHD between populations

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First, all participants completed the Disabilities of the Arm, Shoulder and Hand

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questionnaire (DASH; a 30-item questionnaire that addresses upper limb physical

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disability and symptoms).14 MWU with SCI also completed the Wheelchair User's

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Shoulder Pain Index (WUSPI; a 15-item that provides a personal estimate of shoulder

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pain experienced during general activities).15 Secondly, US measurements of AHD were

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performed in the 5 positions mentioned above. Thereafter, US measurements of the

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supraspinatus tendon thickness were performed.

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Outcome measures

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US measurement of AHD

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US evaluations were performed using MyLab®Five (Esaote Biomedics, Genoa, Italy – in

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Quebec City) and HD11 XE (Philips Medical Systems, Bothell, WA, USA – in Montreal)

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with a 5-12-MHz and a 5-cm wide footprint linear transducer at both locations.8 US

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images of AHD were captured with the participant in a standardized seated position, with

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the feet on the footrests and a neutral spine posture. US measures were taken by placing

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the transducer on the anterior aspect of the lateral surface of acromion along the

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longitudinal axis of the humerus in a frontal plane.8,10 Images were taken when the

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inferior edge of the acromion was optimized, generally around 1cm posterior to the

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acromion anterior angle; thus allowing the visualization of the anterior aspect of the

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subacromial space (Figure 2). The AHD was measured (in mm) using the build-in

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electronic caliper option by manually locating the superior aspect of the humeral head

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and the inferior aspect of acromion, and then measuring the shortest linear distance

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between those two landmarks. For each upper limb position, three measurements were

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taken, but only the mean of the first two was used for statistical analyses. However, if the

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variation between the first two measurements was above 10%, the mean of the three

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AHD measurements was used (as recommended in clinics).8,9 Between measurements,

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patients were instructed to bring their arm down in a resting position to minimize fatigue.

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Change between AHD measured at rest and AHD measured in the four others positions

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(∆AHD 0-45°, ∆AHD 0-MIN°, ∆AHD 0-PEAK°, ∆AHD 0-MAX°) were calculated to

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determine variation in AHD (∆AHD) associated with humeral abduction or propulsion.

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US measurement of supraspinatus tendon thickness

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US images of the supraspinatus tendon were captured with the participants seated, feet on

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the footrests and a neutral spine posture. Participants were asked to place their involved

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hand behind their back (crass position) with the humerus in extension.16 The transducer

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was placed on the anterior aspect of the shoulder, perpendicular to the supraspinatus

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tendon and just anterior to the anterior-lateral margin of the acromion to capture the

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supraspinatus tendon along a short axis (Figure 3). The thickness of the tendon borders

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was defined inferiorly as the first hyperechoic region above the anechoic articular

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cartilage of the humeral head, and the hyperechoic superior border of the tendon before

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the anechoic subdeltoid bursa. Three measurements were taken, but as for AHD, only the

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mean of the first two were used for statistical analyses, except if the variation was above

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10%. Thereafter, mean tendon thickness measured was expressed as a percentage of the

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mean AHD at rest using the following formula: occupation ratio = [(mean tendon

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thickness/mean AHD) x 100]. The occupation ratio highlights the tendon thickness

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relative to the available subacromial space.

150 Data and statistical analysis

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Reliability of US measures of AHD

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In each upper limb position, the intrarater reliability of the AHD and ∆AHD were

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analyzed by comparing the mean of the two measurements (or the mean of the three trial

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if necessary) of the first and the second data collection of the first evaluator. For the

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interrater reliability, the mean of the two first trials (or the mean of the three trial if

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necessary) of the data collection of the first evaluator were compared to the second

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evaluator. Reliability was estimated by calculating the intraclass correlation coefficients

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(ICCs) and its 95% confidence interval (95% CI). ICC values were considered to reflect a

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very poor reliability (ICC < 0.20), a poor reliability (ICC = 0.21-0.40), a moderate

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reliability (ICC = 0.41-0.60), a good reliability (ICC = 0.61-0.80) or an excellent

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reliability (ICC = 0.81-1.00).17 Absolute reliability was assessed with minimal detectable

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change at 90% confidence interval (MDC 90%). The MDC 90% was calculated by

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multiplying the standard error of measurement by the z-score corresponding to the level

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of significance and by the square root of 2.18

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Comparison of US measures of AHD between populations

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To compare US measures of AHD between MWU with SCI with or without RC

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tendinopathy, a 2-way repeated measures ANOVA (2 groups x 5 positions) was

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performed. A Sidak correction was used for post-hoc tests. A 2-way repeated measures

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ANOVA (2 groups x 5 positions) was also used to compare all SCI participants’ as one

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group compared to the able-bodies. Independent t-tests were used to compare MWU with

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SCI with RC tendinopathy to MWU with SCI without RC tendinopathy and MWU with

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SCI to able-bodies for supraspinatus tendon thickness and occupation ratio. All analyses

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were conducted with the Statistical Package for the Social Sciences (SPSS) (version 22

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for Mac; IBM SPSS Software, Armonk, NY, USA). The alpha level was set at 0.05.

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176 RESULTS

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Reliability of US measurements of AHD

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Sixteen MWU with SCI (all without shoulder pain; 12 in Montreal and 4 in Quebec City)

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and 16 able-bodies (8 in each city) took part in Part 1 (Table 1).

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Excellent intra- and interrater reliability was obtained for AHD in each arm position

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(Table 2 and 3), while for ∆AHD the intrarater reliability varied from moderate to

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excellent and the interrater reliability from low to moderate. MDC 90% varied from 0.9

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mm to 3.1 mm for AHD, and from 1.6 mm to 3.8 mm for ∆AHD.

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Comparison of US measurements of AHD between populations

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Sixty-three subjects (37 MWU with SCI [17 with and 20 without RC tendinopathy; 16 in

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Montreal and 21 in Quebec City] and 26 able-bodied individuals [18 in Montreal and 8 in

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Quebec City]) took part in Part 2 (Table 1). Mean DASH score was higher (P<0.003) for

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MWU with RC tendinopathy compared to MWU without shoulder pain. A significant

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difference was also found between MWU with SCI with and without RC tendinopathy in

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WUSPI (P=0.003); MWU with RC tendinopathy experienced more shoulder pain in their

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activity day living.

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194 No significant Group or Group x Position interaction were found for AHD measures

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between MWU with SCI with and without RC tendinopathy. However, a significant

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difference was observed between the two MWU groups in the mean thickness of the

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supraspinatus tendon; MWU without shoulder pain have thicker tendon than MWU with

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RC tendinopathy (P<0.003).

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A significant Group x Position interaction was observed when comparing MWU with

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SCI to able-bodies (P=0.034). The post-hoc analysis shows that AHD measure at MAX

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was greater for the MWU with SCI than able-bodies (Figure 4). Data also showed that

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MWU with SCI have thicker supraspinatus tendon and a higher occupation ratio when

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compared to able-bodies.

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DISCUSSION

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Reliability of US measures of AHD

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US measurements of AHD showed excellent reliability, while the ∆AHD in abduction

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and propulsion was lowly to highly reliable. Previous studies that have assessed the

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intrarater reliability of AHD in able-bodies have reported excellent reliability (ICC: 0.86-

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0.94) with the shoulder at rest (0° of elevation)19-24 and good to excellent reliability (ICC:

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0.76-0.88) with the shoulder at 45° of abduction.22,23 Most of these studies used, as in the

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present study, a mean of 222 or 320,23,24 measures for the calculation of reliability indices

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(not mentioned in 3 studies).19,21,23,25 However, using the mean of 3 measures has not

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been shown to impact the relative (ICC) and absolute (MDC) reliability of US

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measurements when compared to the mean of 2 measures.26,27 A recent study by Lin et al.

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also evaluated the intra- and interrater reliability of US measurement of AHD of MWU

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with SCI at rest and at 45° and 90° of abduction and obtained good to excellent

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reliability.28 However, they did not look at propulsion positions.

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Similarly to our study, Desmeules et al. showed that interrater reliability of AHD

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measurements was excellent in able-bodies at rest (ICC=0.86), at 45° (ICC=0.91) and 60°

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(ICC=0.92) of abduction. In contrast, Pijls and al. obtained lower interrater reliability

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indices with the shoulder at rest (ICC=0.70) and at 60° of abduction (ICC=0.64).20 This

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discrepancy may be explained by the fact that our study and the one by Desmeules et al.29

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included mostly young participants without shoulder pain (mean age of 31 and 34 years,

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respectively), while participants in Pijls et al. study were older (mean age: 52 years) and

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had subacromial pain. In patients with subacromial pain, the lower border of the

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acromion may be difficult to recognize due to the inflammatory reaction of the soft

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tissues.20

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Finally, in our study, intra- and interrater reliability was much lower for ∆AHD compared

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to AHD, and the MDC 90% represented a higher percentage of the total score. Given that

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two measurements are required to determine the variation in abduction or in propulsion,

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the variability of a difference between two measurements is higher than the variability of

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a single measurement, increasing the risks of measurement errors. This measure is

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therefore not recommended in clinics.

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Between-group differences for US measures of AHD and supraspinatus tendon

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We found that MWU without shoulder pain have thicker tendon than MWU with RC

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tendinopathy, and that the mean AHD at the end of push phase is larger in MWU with

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SCI compared to able-bodies, while the supraspinatus tendon is significantly thicker and

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occupies a significantly larger part of the outlet in MWU with SCI. It could be

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hypothesized that a larger AHD could be an adaptation for an increased tendon thickness

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to normalize the tendon ratio within the outlet and protect its integrity. This potential

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adaptation would be similar to the one observed in athletes. Maenhout et al. found that

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overhead athletes present increased AHD on their dominant sides, where tendons are also

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found to be thicker.30 Wang et al. found a greater AHD and a thicker supraspinatus

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tendon in elite baseball athletes compared to controls.21 In these populations, shoulder

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muscles are overused in comparison to the normal population, which could explain the

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thickening of the tendon. In our study, the thickness of the tendon in MWU without pain

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may represent specific adaptation that may explain why this group does not suffer from

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pain. Therefore, the tendon of MWU without shoulder pain might be better adapted to

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manual wheelchair propulsion then those without pain.

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The occupation ratio was used to define the relationship between tendon thickness and

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AHD. Our results suggest the AHD alone may not be enough to explain how the AHD is

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occupied and that the occupation ratio gives a better overview of the subacromial space.

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A thicker supraspinatus tendon and a greater tendon occupation ratio was observed in

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able-bodies with subacromial pain and suggested a potential extrinsic mechanism of

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compression of the tendon.10 However, in the present study, such difference between

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MWU with SCI with and without pain was not shown, which could be explained by the

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increased thickness of the supraspinatus tendon in MWU without shoulder pain.

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In our study, a greater AHD was specifically observed at the end of wheelchair

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propulsion cycle between MWU and able-bodies. This position corresponds to the end of

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the push phase in the push-off arm position. In this position, the shoulder is positioned at

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around 20° of flexion. In fact, it is the only positioned measured in which the upper limb

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is elevated during propulsion. It may explain that it was the only position in which a

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difference was observed.

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Firstly, while the scapular and trunk positions were standardized during the US

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assessments, they were not measured. Therefore, they may have impacted our results

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given their influence on shoulder kinematics. Additional evaluation of the scapula and

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trunk should be considered in future investigations. Secondly, thickness of the

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supraspinatus tendon and AHD were not measured in similar anatomical positions. Since

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AHD is influenced by glenohumeral and scapulothoracic kinematics, this ratio only

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represents an estimation of the percentage of occupation. Thirdly, shoulder x-rays were

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not performed. Therefore, the presence of glenohumeral osteoarthritis or calcific

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tendinosis could not be excluded. Finally, the fact that MWU without shoulder pain

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reported some upper limb disabilities on the DASH could explain the lack of the

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between-groups differences for MWU with and without RC tendinopathy.

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CONCLUSION

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We demonstrated that US is a reliable mean to evaluate the AHD in MWUs with SCI in

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the three propulsion positions assessed. Our results suggest that measurement of the

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supraspinatus tendon thickness and its occupation ratio are significantly different between

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MWU with SCI and able-bodies, suggesting adaptation to the tendon associated with an

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increase of use. Future studies are needed to better understand the impact of the changes

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in AHD and supraspinatus tendon thickness in SCI populations.

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Lundqvist C, Siosteen A, Blomstrand C, Lind B, Sullivan M. Spinal cord injuries. Clinical, functional, and emotional status. Spine (Phila Pa 1976). 1991;16(1):7883. Akbar M, Brunner M, Balean G, et al. A cross-sectional study of demographic and morphologic features of rotator cuff disease in paraplegic patients. Journal of shoulder and elbow surgery / American Shoulder and Elbow Surgeons ... [et al.]. 2011;20(7):1108-1113. Gutierrez DD, Thompson L, Kemp B, et al. The relationship of shoulder pain intensity to quality of life, physical activity, and community participation in persons with paraplegia. The journal of spinal cord medicine. 2007;30(3):251255. Akbar M, Balean G, Brunner M, et al. Prevalence of rotator cuff tear in paraplegic patients compared with controls. The Journal of bone and joint surgery. American volume. 2010;92(1):23-30. Hastings J, Goldstein B. Paraplegia and the shoulder. Phys Med Rehabil Clin N Am. 2004;15(3):vii, 699-718. Curtis KA, Drysdale GA, Lanza RD, Kolber M, Vitolo RS, West R. Shoulder pain in wheelchair users with tetraplegia and paraplegia. Arch Phys Med Rehabil. 1999;80(4):453-457. Alm M, Saraste H, Norrbrink C. Shoulder pain in persons with thoracic spinal cord injury: prevalence and characteristics. J Rehabil Med. 2008;40(4):277-283. Desmeules F, Minville L, Riederer B, Cote CH, Fremont P. Acromio-humeral distance variation measured by ultrasonography and its association with the outcome of rehabilitation for shoulder impingement syndrome. Clinical journal of sport medicine : official journal of the Canadian Academy of Sport Medicine. 2004;14(4):197-205. Savoie A, Mercier C, Desmeules F, Fremont P, Roy JS. Effects of a movement training oriented rehabilitation program on symptoms, functional limitations and acromiohumeral distance in individuals with subacromial pain syndrome. Man Ther. 2015. Michener LA, Subasi Yesilyaprak SS, Seitz AL, Timmons MK, Walsworth MK. Supraspinatus tendon and subacromial space parameters measured on ultrasonographic imaging in subacromial impingement syndrome. Knee surgery, sports traumatology, arthroscopy : official journal of the ESSKA. 2015;23(2):363369. Michener LA, Walsworth MK, Doukas WC, Murphy KP. Reliability and diagnostic accuracy of 5 physical examination tests and combination of tests for subacromial impingement. Arch Phys Med Rehabil. 2009;90(11):1898-1903. Ngomo S, Mercier C, Bouyer LJ, Savoie A, Roy JS. Alterations in central motor representation increase over time in individuals with rotator cuff tendinopathy. Clin Neurophysiol. 2015;126(2):365-371. Rice I, Gagnon D, Gallagher J, Boninger M. Hand rim wheelchair propulsion training using biomechanical real-time visual feedback based on motor learning theory principles. The journal of spinal cord medicine. 2010;33(1):33-42.

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Hudak PL, Amadio PC, Bombardier C. Development of an upper extremity outcome measure: the DASH (disabilities of the arm, shoulder and hand) [corrected]. The Upper Extremity Collaborative Group (UECG). Am J Ind Med. 1996;29(6):602-608. Curtis KA, Roach KE, Applegate EB, et al. Development of the Wheelchair User's Shoulder Pain Index (WUSPI). Paraplegia. 1995;33(5):290-293. Shah NP, Miller TT, Stock H, Adler RS. Sonography of supraspinatus tendon abnormalities in the neutral versus Crass and modified Crass positions: a prospective study. Journal of ultrasound in medicine : official journal of the American Institute of Ultrasound in Medicine. 2012;31(8):1203-1208. Portney LG, Watkins MP. Foundation of clinical research: Applications to practice. 3rd ed. Upper Saddle River, NJ: Pearson Prentise Hall; 2009. Portney L, Watkins M. Statistical Measures of Validity. Foundations of Clinical Research- Applications to Practice. 3rd ed. Upper Saddle River2009:619-658. Schmidt WA, Schmidt H, Schicke B, Gromnica-Ihle E. Standard reference values for musculoskeletal ultrasonography. Ann Rheum Dis. 2004;63(8):988-994. Pijls BG, Kok FP, Penning LI, Guldemond NA, Arens HJ. Reliability study of the sonographic measurement of the acromiohumeral distance in symptomatic patients. Journal of clinical ultrasound : JCU. 2010;38(3):128-134. Wang HK, Lin JJ, Pan SL, Wang TG. Sonographic evaluations in elite college baseball athletes. Scand J Med Sci Sports. 2005;15(1):29-35. Kalra N, Seitz AL, Boardman ND, 3rd, Michener LA. Effect of posture on acromiohumeral distance with arm elevation in subjects with and without rotator cuff disease using ultrasonography. The Journal of orthopaedic and sports physical therapy. 2010;40(10):633-640. Maenhout A, van Cingel R, De Mey K, Van Herzeele M, Dhooge F, Cools A. Sonographic evaluation of the acromiohumeral distance in elite and recreational female overhead athletes. Clinical journal of sport medicine : official journal of the Canadian Academy of Sport Medicine. 2013;23(3):178-183. White CE, Dedrick GS, Apte GG, Sizer PS, Brismee JM. The effect of isometric shoulder internal and external rotation on the acromiohumeral distance. American journal of physical medicine & rehabilitation / Association of Academic Physiatrists. 2012;91(3):193-199. Maenhout A, Dhooge F, Van Herzeele M, Palmans T, Cools A. Acromiohumeral Distance and 3-Dimensional Scapular Position Change After Overhead Muscle Fatigue. Journal of athletic training. 2015. Skou ST, Aalkjaer JM. Ultrasonographic measurement of patellar tendon thickness--a study of intra- and interobserver reliability. Clin Imaging. 2013;37(5):934-937. Drolet PM, MD. Lacroix, MD and Roy, Jean-Sebastien. Reliability of ultrasound evaluation of the long head of the biceps tendon. Journal of Rehabilitation Medicine 2016. Lin YS, Boninger ML, Day KA, Koontz AM. Ultrasonographic measurement of the acromiohumeral distance in spinal cord injury: Reliability and effects of shoulder positioning. The journal of spinal cord medicine. 2014.

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Desmeules F, Minville L, Riederer B, Cote CH, Fremont P. Acromio-humeral distance variation measured by ultrasonography and its association with the outcome of rehabilitation for shoulder impingement syndrome. Clinical journal of sport medicine : official journal of the Canadian Academy of Sport Medicine. 2004;14(4):197-205. Maenhout A, Van Eessel V, Van Dyck L, Vanraes A, Cools A. Quantifying acromiohumeral distance in overhead athletes with glenohumeral internal rotation loss and the influence of a stretching program. The American journal of sports medicine. 2012;40(9):2105-2112.

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Table 1 Participants’ characteristics MWU with SCI without

shoulder pain

shoulder pain

(n = 17)

(n = 20)

Gender - Male, n (%)

14 (82)

Weight, kg, X±SD

68±11

Height, cm, X±SD

172±14

Years since the injury AIS, A/B/C/D, %

Able-bodied (n = 26)

45±10

31±5

17 (85)

17 (65)

84±30

89±14

172±15

175±12

27±12

16±13

-

28/9/14

36/4/9

-

Level of injury, %, lower cervical (C5-C7)

10

20

-

Level of injury, %, mid thoracic (T3-T8)

53

33

-

37

47

-

27±13 *

14±11

2±2

24±17 *

5±4

-

2±2

0

0

4±2

0

0

3±2

0

0

WUSPI, /100, X±SD VAS - Pain at rest, /10, X±SD

VAS - Pain at night, /10, X±SD

AC C

VAS - Pain during ADL, /10, X ±SD

TE D

DASH, /100, X±SD

EP

Level of injury, %, lower thoracic (T9-T12)

SC

47±11

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Age, years, X±SD


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MWU with SCI with

ADL: Activity of daily living, DASH: Disabilities of the Arm, Shoulder and Hand, WUSPI: Wheelchair User's Shoulder Pain Index, VAS: Visual analog scales, ASI: Association Impairment Scale, * significant difference (p < 0.05) between MWU with and without shoulder pain

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AHD Evaluator 2

Arm at rest

10.5 +/- 2.6 mm

10.8 +/- 3.3 mm

0-45°

ABD 45°

9.1 +/- 3.4 mm

8.1 +/- 3.5 mm

0-MIN°

MIN

11.6 +/- 3.4 mm

11.0 +/- 3.0 mm

PEAK

10.6 +/- 3.0 mm

10.6 +/- 3.4 mm

MAX

9.8 +/- 3.4 mm

10.0 +/- 3.6 mm

∆AHD

Evaluator 1

Evaluator 2

-1.3 +/- 2.1 mm

-2.7 +/- 1.9 mm

1.1 +/- 1.8 mm

0.2 +/- 1.5 mm

0-PEAK°

0.1 +/- 1.4 mm

-0.2 +/-1.5 mm

0-MAX°

-0.6 +/- 1.8 mm

-0.8 +/- 1.9 mm

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Table 2 - Acromiohumeral distance at T1 for the two evaluators

AHD: Acromiohumeral distance, ∆AHD: Change between AHD measured at rest and AHD measured in the others positions, Arm at

TE D

rest: 0° of arm elevation, ABD 45; 45° of active shoulder abduction with elbow at 90° of flexion, MIN: shoulder at 30° of extension,

AC C

EP

PEAK: shoulder at 0° of flexion, MAX: shoulder at 20° of flexion.

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Table 3 - Reliability of US measures of AHD AHD

ICC (95% CI)

RI PT

Intrarater

∆AHD Interrater

MDC90 %

Intrarater

ICC (95% CI)

MDC90%

Interrater

ICC (95% CI)

MDC90%

ICC (95% CI)

MDC90%

0.64 (0.27-0.83)

2.8 mm

0.40 (-0.13-0.70)

3.8 mm

0.84 (0.67-0.92)

1.6 mm

0.44 (-0.14-0.69)

3.1 mm

0.98 (0.95-0.99)

0.9 mm

0.94 (0.87-9.71)

1.7 mm

0-45°

ABD 45°

0.86 (0.71-0.93)

3.0 mm

0.85 (0.68-0.93)

3.1 mm

0-MIN°

MIN°

0.95 (0.91-0.98)

1.6 mm

0.94 (0.86-0.97)

1.8 mm

0-PEAK°

0.61 (0.17-0.81)

2.1 mm

-0.28 (-1.00-0.39)

3.8 mm

PEAK°

0.94 (0.88-0.97)

1.7 mm

0.94 (0.87-0.97)

1.8 mm

0-MAX°

0.73 (0.43-0.87)

2.0 mm

0.60 (0.17-0.81)

2.7 mm

MAX°

0.96 (0.91-0.98)

1.5 mm

0.95 (0.91-0.98)

1.7 mm

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Arm at rest

ICC: Intraclass correlation coefficient, MDC: Minimal detectable change, 95% CI: 95% confidence interval, AHD: Acromiohumeral distance, ∆AHD: Change between AHD measured at rest and AHD measured in the others positions, Arm at rest: 0° of arm elevation,

AC C

flexion, MAX: shoulder at 20° of flexion

EP

ABD 45; 45° of active shoulder abduction with elbow at 90° of flexion, MIN: shoulder at 30° of extension, PEAK: shoulder at 0° of

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Fig 4.

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Figure Legends Fig 1. Five static upper limb positions of US measures of AHD; A- arm at rest, B- 45° of AHD, C- MIN position, D- PEAK position, E- MAX position

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Fig 2. Ultrasonographic measurement of AHD Fig 3. Ultrasonographic measurement of supraspinatus tendon thickness

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Fig 4. Acromiohumeral distance according to group and positions. Error bars indicate standard deviations.