Accepted Manuscript Title: Investigation of supraspinatus muscle architecture following concentric and eccentric training Author: Soo Y. Kim Jong Bum Ko Jonathan P. Farthing Scotty J. Butcher PII: DOI: Reference:

S1440-2440(14)00090-5 http://dx.doi.org/doi:10.1016/j.jsams.2014.05.007 JSAMS 1034

To appear in:

Journal of Science and Medicine in Sport

Received date: Revised date: Accepted date:

29-10-2013 1-5-2014 11-5-2014

Please cite this article as: Kim SY, Ko JB, Farthing JP, Butcher SJ, Investigation of supraspinatus muscle architecture following concentric and eccentric training, Journal of Science and Medicine in Sport (2014), http://dx.doi.org/10.1016/j.jsams.2014.05.007 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.

*Title page (including all author details and affiliations)

Investigation of supraspinatus muscle architecture following concentric and eccentric training Soo Y. Kima, Jong Bum Kob, Jonathan P. Farthingc, Scotty J. Butchera a

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School of Physical Therapy, 1121 College Drive, University of Saskatchewan, Saskatoon, Saskatchewan, S7N 0W3, Canada b Present address, Department of Physiology, 107 Wiggins Road, University of Saskatchewan, Saskatchewan, S7N 5E5, Canada c College of Kinesiology, 87 Campus Drive, University of Saskatchewan, Saskatchewan, S7N 5B2, Canada

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Address for correspondence: Soo Y. Kim School of Physical Therapy, College of Medicine University of Saskatchewan 1121 College Drive, Saskatoon, Saskatchewan, Canada S7N 0W3

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Corresponding author: Soo Y. Kim

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Email: [email protected]

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Word count: 2988 Abstract word count: 250 Number of Tables: 3

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*Manuscript (excluding all author details and affiliations)

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Investigation of supraspinatus muscle architecture following concentric and eccentric training

2 Abstract

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Objectives: To investigate the effects of concentric or eccentric abduction strength training on

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supraspinatus fiber bundle architecture and strength. Design: A pre- post single-subject design. Method:

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Thirteen participants were randomized to concentric (n=6) or eccentric (n=7) training groups.

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Participants completed an eight week shoulder abduction training program in the scapular plane using an

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isokinetic dynamometer. Resistance training, requiring maximal effort on contraction, consisted of 4 sets

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of 8 reps at 60 degrees/sec in weeks 1-4, and 6 sets of 6 reps at 60 degrees/sec in weeks 5-8 with a

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frequency of 3x/week. Primary outcome measures included fiber bundle length, pennation angle, and

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muscle thickness of supraspinatus and these were quantified using ultrasound. Secondary outcome

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measures included isometric, eccentric and concentric abduction strength and these were evaluated using

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the isokinetic dynamometer. Results: Mean fiber bundle length in the relaxed (p=0.033) and contracted

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(p=0.036) states significantly decreased with concentric training but remained unchanged with eccentric

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training. A significant increase in pennation angle, muscle thickness, and peak torque were found with

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training but no significant differences were detected between concentric and eccentric groups.

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Conclusions: Training mode has a significant impact on fiber bundle length changes of the supraspinatus.

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Eccentric training of shoulder abduction leads to similar strength gains as concentric, but it may also have

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the added advantages of maintaining fiber bundle lengths and promoting tendon healing. Study is needed

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to confirm fiber bundle changes in a clinical population which would further support the use of eccentric

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abduction strength training in rehabilitation settings.

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Key words: rotator cuff, exercise, shoulder, fiber bundle, torque, rehabilitation

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Introduction The supraspinatus is one of the four rotator cuff muscles of the shoulder and plays an important

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role in dynamic stabilization of the humeral head within the glenoid fossa.1 The muscle is involved in

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both abduction and external rotation of the shoulder.2,3 Among the rotator cuff muscles, supraspinatus is

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most frequently involved with impingement syndrome and tendinopathy.4 Studies have found 16-40% of

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all shoulder complaints are linked with impingement related tendinopathies, which are often the precursor

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for rotator cuff tears.52

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Tendinopathies of the supraspinatus are commonly treated conservatively.

Treatment may

consist of muscle and tendon stretches along with retraining and strengthening of the rotator cuff and

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scapular muscles.6,7 Common strengthening exercises for the supraspinatus often include shoulder

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abduction activities1 and may involve concentric or eccentric activities. Concentric training involves

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active muscle contraction against an external load that leads to shortening of the muscle fibers. In

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contrast, eccentric strength training involves active muscle contraction against a load that is greater than

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the force produced by the muscle and leads to lengthening of the muscle fibers.

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Eccentric exercises are not only effective for strength gains and muscle hypertrophy8 but also for

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promoting tendon healing. A decrease in tendon thickness has been found following eccentric training9

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and the high loads stimulate collagen synthesis and promote revascularization.10,11

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training is used clinically to treat tendinopathies of the lower extremity.

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training may also be beneficial for treating tendinopathies of the rotator cuff; similarities in histologic

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changes of the tendon have been found between lower extremity tendinopathies and the supraspinatus. 12

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Improvements in upper extremity physical function and pain have been reported following eccentric

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strength training protocols involving shoulder abduction and external rotation.13

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As such, eccentric

Research suggests eccentric

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To date, few studies have investigated the effects of eccentric or concentric training on muscle

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architecture in humans which is a primary determinant of muscle function.14 The length of the fiber

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bundles (FBL) and the pennation angles (PA) have a direct impact on the maximum force producing 2 Page 3 of 20

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capabilities of a muscle. A 20% increase in FBL can increase the maximum force by 25%.15 To our

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knowledge, the impact of training on the fiber bundle architecture of supraspinatus has not been

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investigated. Therefore, the purpose of this study was to investigate the effects of an 8 week isokinetic

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concentric or eccentric abduction strength training program on (1) the fiber bundle architecture of

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supraspinatus using a previously validated ultrasound imaging protocol16 and (2) on isometric and

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dynamic strength. We hypothesized the training mode would significantly influence FBL, PA, muscle

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thickness (MT) and peak torque changes. Findings from this study could aid in improved clinical practice

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guidelines for patients with supraspinatus tendinopathies and perhaps position patients for better surgical outcomes if conservative management fails.

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Methods

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Fourteen recreationally active participants between the ages of 18-50 years volunteered for this

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study. Exclusion criteria included any previous or present rotator cuff pathology, glenohumeral joint

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instability, neuromuscular disease, or any other condition that may have limited participants’ ability to

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perform the required shoulder exercises. One participant did not complete the study due to personal

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reasons. Thus, the final group of participants (7 female and 6 male) had a mean age of 28.2±8.3 years.

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All participants were adequately informed about the study, which was approved by the Biomedical Ethics

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Research Board at the University of Saskatchewan (Bio#11-51). Written informed consent was obtained

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prior to any data collection.

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Participants were permitted to maintain regular physical activity, as long as the intensity was not

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altered during the course of the study. Measurements of weight and height were recorded. Table 1

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provides a summary of participants’ characteristics.

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This was a randomized pre- post single-subject design. Following adequate orientation to the

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study procedures, ultrasound scans of the supraspinatus muscle and abduction strength measurements of

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the right arm were obtained using the protocols outlined in the sections below. Participants were

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randomly assigned into either the concentric or eccentric shoulder abduction training groups. Ultrasound

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scans and abduction strength measures were repeated at the end of the eight week training program.

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The ultrasound protocol outlined by Kim et al.16 was used for this study.

The reliability and

validity has been previously established. A LOGIQ e BT08 GE Healthcare Scanner (GE Medical

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Systems, Milwaukee, Wisconsin, USA) with a 12 MHz linear array (38 mm) transducer was used. All

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images were taken by the principal investigator (S.Y.K) who was trained in musculoskeletal ultrasound

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imaging for supraspinatus.

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Participants were seated in an upright chair with a backrest during the scanning session. The

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orientation of the transducer was kept perpendicular to the plane of the fiber bundles being captured. The

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anterior region of the supraspinatus was imaged in three different positions: relaxed 0° abduction (arm

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resting by the side of chair), relaxed 60° abduction (arm supported by a pillow), and contracted

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(isometric) 60° abduction. A universal goniometer was used to accurately position the limb. In each arm

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position, 10-20 ultrasound images were taken. Coronal panoramic images were used to scan fiber

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bundles within the middle part of the anterior region. Sagittal scans taken at the mid-point of the muscle

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belly were used to capture MT. Care was taken not to deform the underlying tissues by using minimum

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pressure required to take a clear image. All images were saved for subsequent analyses.

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All quantitative measurements from ultrasound images were made by the principal investigator

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(S.Y.K) who was blinded to the training protocol of the participants. Images with clearly visible fiber

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bundles that could be seen for most of their length and at their medial and lateral attachment sites were

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used for analysis. As outlined by Kim et al.16, FBL was measured as the linear distance between the

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medial and lateral attachment sites (Fig. 1). Pennation angle was measured as the angle between the fiber

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bundle and its attachment to the intramuscular tendon (Fig. 1). Muscle thickness, the distance between

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the superficial surface of the muscle and the supraspinatus fossa, was measured at the midpoint of the

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muscle belly length. 17

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An isokinetic dynamometer (Humac NORM dynamometer, CSMi, Stoughton, MA, USA) was

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used to test shoulder abduction strength in the scapular plane.

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exercises which included 10 repetitions of shoulder abduction at ~50% maximum effort. Following this,

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maximum isometric abduction strength was measured at 60° abduction. Participants were instructed to

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hold the contraction for three seconds. Each participant performed three repetitions with three minutes of

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rest between each trial. Next, maximum eccentric abduction strength was measured between 20°-100°

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followed by concentric. Strength, measured as peak torque output, was calculated for each participant

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based on the maximum force production over the course of these repetitions.

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Each participant was given warm-up

The intervention consisted of eight weeks of training, with three 15-minute sessions, per week. A

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minimum of 48 hours separated each session. Participants performed either eccentric or concentric

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abduction exercises in the scapular plane using the isokinetic dynamometer, according to the strength

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training group they were assigned to. For convenience, only the right arm was trained. In first phase

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(weeks 1-4), participants performed 4 sets of 8 repetitions at 60°/sec using maximal effort. In second

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phase (weeks 5-8), participants performed 6 sets of 6 repetitions at 60°/sec at maximal effort. One minute

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of rest was provided between sets for both training groups.

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Each participant was securely strapped into the seat to minimize movement of the trunk and any

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compensatory techniques. The position of the seat, backrest and lever arm for each participant was

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recorded and kept consistent.

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provided verbal encouragement with each repetition.

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All training sessions were conducted by one research assistant that

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All parameters were imported into SPSS (version 20; SPSS Inc., Chicago, IL, USA). Each

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parameter was characterized with descriptive statistics (mean, standard deviation, and range). Student’s

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unpaired t-tests were used to compare differences in age, physical characteristics and measured variables

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between training groups at baseline. A 2 X 2 factorial analysis of variance (ANOVA) was used to test for

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differences in time (pre- vs. post training) and training group (eccentric vs. concentric) for all measured

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variables (FBL, PA, MT and peak torque). Simple effects analysis and post hoc testing using multiple

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comparisons was used where necessary. Statistical significance was set at p0.05). See Table 1. In addition, no differences were

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found for all architectural parameters and peak torque values between the training groups at baseline

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(p>0.05). Table 2 provides a summary of architectural measures pre- and post-training for both groups

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and Table 3 a summary of peak torque values. There were no adverse events or injuries with the training

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protocol.

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(p=0.033) in the neutral relaxed state.

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For FBL, there was a significant group X time interaction (p=0.003) and a main effect for time Mean FBL in the concentric group significantly decreased

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following training (p=0.007) whereas no significant change was found in the eccentric group (p>0.05).

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With the arm passively abducted to 60°, mean FBL decreased following training for both groups pooled

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(p=0.047) with no significant differences between groups (p>0.05). With the arm actively abducted to

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60°, there was a significant group X time interaction (p=0.009). Similar to the relaxed state, mean FBL in

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the concentric group was significantly reduced following training (p=0.036), but no changes were found

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in the eccentric group (p>0.05).

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Mean PA (groups pooled) significantly increased following training with all arm positions tested:

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neutral relaxed state (p=0.030), arm passively abducted to 60° (p=0.002), arm actively abducted to 60°

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(p=0.025). No significant group differences were found (p>0.05).

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Following training, mean MT (groups pooled) significantly increased, but no significant differences were found between the eccentric and concentric training groups (p>0.05).

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For the analysis of peak torque data, one significant outlier was removed from the eccentric

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training group since the relative change in peak torque was more than 85%, which exceeded 4 standard

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deviation units away from the mean relative change for the eccentric group. Peak isometric, concentric

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and eccentric torque values (groups pooled) significantly increased with training (p0.05).

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Discussion 6 Page 7 of 20

This study investigated the architectural changes of the supraspinatus muscle following resistance

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training, which is an integral part of rehabilitative management for tendinopathies and tendon tears of the

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rotator cuff. Following an eight week abduction resistance training program for supraspinatus, significant

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differences in the fiber bundle architecture and strength were found. Further, significant differences in

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the change in FBL were identified when comparing eccentric and concentric training. Findings from this

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study (1) confirm one of our hypotheses that training mode can impact the type of FBL changes in the

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supraspinatus and (2) suggest eccentric training of the supraspinatus aids in maintaining FBL which may

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be beneficial in clinical populations.

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The mode of contraction with resistance training had a significant impact on FBL changes within

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the supraspinatus muscle. The concentrically trained participants showed a significant decrease in mean

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FBL, observed in both the relaxed and contracted states of the muscle, whereas for the eccentrically

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trained participants FBL was maintained. Similar findings were reported by Butterfield et al.

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animal study, where a significant decrease in the number of sarcomeres of the vastus lateralis muscle was

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shown in the concentric group, while no changes were noted in the eccentric group. Contrary to these

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findings, previous training studies of the human vastus lateralis have reported significant increases in FBL

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with either training mode. Blazevich et al 19, for example, reported a similar increase in FBL of the vastus

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lateralis between concentrically and eccentrically trained participants. In studies where the training

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program incorporated a combination of both concentric and eccentric resistance, mean FBL also

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significantly increased post training.20,21 Potier et al.22 also found an increase in FBL following an eight

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week eccentric training program for the biceps femoris; however, the changes were not significant

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between the controls.

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Discrepancies in FBL changes found in the current study and those of the lower limb may be

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attributed to functional differences in the muscles. Both the quadriceps and hamstrings are large prime

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movers of the lower extremity. Butterfield et al.18 found differences in sarcomere adaptations even within

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different parts of the quadriceps muscle following training suggesting that FBL changes may not only be

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muscle specific but also regionally specific within an individual muscle.

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influence these differences is the mechanical properties of the tendon and aponeuroses.23 Studies have

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reported an increase in tendon stiffness following resistance training.24 The supraspinatus tendon which

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coalesces with the other rotator cuff tendons may have tendon properties different from those of the lower

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limbs. In addition, the anterior region of the supraspinatus muscle, which was investigated in the present

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study, is circumpennate in architecture with a long intramuscular portion of the tendon extending

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medially into the muscle belly. The vastus lateralis and biceps femoris, on the other hand, are bipennate.

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The difference in fiber bundle architecture and the mechanical properties of the tendon could have

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contributed to the study findings and should be further investigated in future studies.

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Another factor that may

The maintenance of FBLs with eccentric training, in comparison to shortened FBL with

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concentric training in this present study may be of functional significance. Changes in FBL are known to

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have a profound impact on both static and dynamic properties of a muscle.25 The preservation of FBL

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along with a concurrent increase in strength with eccentric training, as observed in this study, suggests the

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supraspinatus muscle is able to sustain force over a greater range compared to when the muscle is trained

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concentrically. This combination of changes may be ideal for rotator cuff muscles such as supraspinatus

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where providing dynamic stability of the glenohumeral joint within a large range of motion is important.

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Although future studies on clinical populations are needed, the FBL findings of this study may also be of

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clinical significance. Given that eccentric training promotes tendon healing in the Achilles and patellar

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tendons10,11 and possibly that of the rotator cuff12, this training mode may have the added benefit of

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healing microtrauma of the supraspinatus tendon caused from various functional and/or sports activities.

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Furthermore, the length of the muscle is an important predictor for surgical outcomes for rotator cuff

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tears. Retracted and shortened musculotendinous units are more difficult to repair and often have inferior

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outcomes.26 Since supraspinatus tendinopathies often do not respond to conservative management and

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eventually progress into a tear, eccentric training may be more beneficial by maintaining FBL thus

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positioning the muscle architecture for better surgical success.

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Muscle thickness is a common measurement used to indicate muscle hypertrophy after training. 8

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In pennated muscles, hypertrophy is associated with an increase in PA.27 An increase in PA can in turn

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affect the force producing capability of the muscle by allowing a greater amount of contractile tissue to

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attach to a given area of tendon which in turn can lead to a larger physiological cross sectional area.

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Although numerous studies have found that muscle hypertrophy is greater after eccentric training or

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coupled concentric/eccentric training than after concentric training alone,8,28 our study did not find group

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differences in MT. Similar to MT, PA increased significantly with shoulder abduction training, but no

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group differences were found. Further testing with a larger number of participants may be better able to

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determine the influence of training mode on PA changes in supraspinatus.

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Improvements in muscle strength and torque are known to be the result of an increase in neural

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activation and muscle hypertrophy.29 Overload is the proposed stimulus for these muscular and neural

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adaptations. Eccentric muscle contractions are also accepted to result in greater overload. 30 Theoretically,

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eccentric training should result in greater force generation and proportionately greater improvements in

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strength than concentric training alone.29 Our study findings do not directly support this hypothesis. While

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peak torque values increased significantly between pre- and post-testing, no significant group differences

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were found. In many studies, significant differences in concentric and eccentric peak torque were related

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to the type of training the participants received. For example, Blazevich et al. 19 testing the quadriceps

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found that concentric torque was greater in the concentric group than the eccentric while no differences

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were found in eccentric torque. In contrast, Higbie et al.29 found eccentric torque to be greater in the

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eccentric group as well as concentric torque in the concentric group.

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The absolute and relative loads on the muscle with our training protocol may have contributed to

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the discrepancies between our findings and previous literature related to torque. Seger et al.30 suggests

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the absolute load applied to a muscle may not be the same relative load depending on the type of muscle

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contraction. This discrepancy in absolute and relative load could result in the eccentric load being much

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less than the concentric. Although study participants were asked to exert maximal effort during the 9 Page 10 of 20

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training and testing sessions, there may have been differences in the absolute load. Additionally, for

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convenience the right arm was tested and trained regardless of arm dominance.

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Conclusion The findings of this study suggest changes in muscle architecture and morphology evoked by

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resistance training are closely coupled. Since the structure of a muscle best reflects its functional

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demands14, in instances of pathology, the maintenance or restoration of architectural parameters favorable

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to its function is of the utmost importance in rehabilitation. Clinically, the exercise position used in this

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study, abduction in the scapular plane with external rotation, is commonly used.1

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supraspinatus eccentrically in this position could be easily implemented in rehabilitation settings.

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However, abduction in prone lying3 and external rotation2 are also shown to activate the supraspinatus

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and are frequently used clinically. Future studies should investigate the fiber bundle changes associated

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with training mode for these exercises. In addition, studies on a clinical population may be able to further

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inform rehabilitative strategies and surgical practice.

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Practical Implications

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Training mode is associated with muscle fiber bundle length changes of the shoulder

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Eccentric training of the supraspinatus has benefits to both the muscle architecture and tendon

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Eccentric training may be an ideal training mode for rotator cuff tendinopathies

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Acknowledgements

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The authors express appreciation to the Saskatchewan Health Research Foundation for funding

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parts of this study and Laurie Harder, Kristen Moore, Cara-lee Nel, Erica Yuzak, and Stephanie Zacharuk,

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students of the Masters of Physical Therapy program at the School of Physical Therapy, University of

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Saskatchewan, for their assistance with data collection.

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human pennate muscle in response to strength training: Changes in muscle architecture. J Physiol

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28. Ohagan FT, Sale DG, Macdougall JD, et al. Comparative effectiveness of accommodating and weight

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resistance training modes. Med Sci Sports Exerc 1995;27(8):1210-1219.

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29. Higbie EJ, Cureton KJ, Warren GL 3rd, et al. Effects of concentric and eccentric training on muscle

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strength, cross-sectional area, and neural activation. J Appl Physiol 1996;81(5):2173-2181.

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30. Seger JY, Thorstensson A. Effects of eccentric versus concentric training on thigh muscle strength

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and EMG. Int J Sports Med 2005;26(1):45-52.

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Figure 1. Coronal panoramic image of right supraspinatus in the relaxed state. A single fiber bundle in middle part of the anterior region (AM) has been demarcated by a solid white line with two arrow heads. The dotted line represents the intramuscular tendon. Pennation angle (*), fiber bundle length (FBL) and the supraspinous fossa (SF) are labelled.

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Table 1. Summary of Participant Characteristics

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Eccentric n=7 Concentric n=6 Sex 3F, 4M 4F, 2M Age (yrs) 32.4 ±9.3 23.7 ±3.5 Height (cm) 172.1±7.1 168.8±8.9 Weight (kg) 72.9±11.1 63.0±10.4 Values are means ± SD.; n, number of participants

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Table 2. Summary of Architectural Variables for Eccentric and Concentric Training Groups Concentric (n=6) Pre-training Post-training

5.1±0.4 5.1± 0.7 4.8± 0.4

5.4±0.7 5.0 ±0.8 4.7± 0.7

PA (degrees) Neutral/Relaxed* 60° Abd/Relaxed* 60° Abd/ Active*

14.5±5.5 13.3± 5.4 16.5± 2.2

16.8±6.4 18.4± 4.3 19.9± 2.2

13.4±3.0 16.4± 2.6 20.1± 4.0

MT (cm) Neutral/Relaxed*

1.6±0.4

1.8± 0.40

Values are means ± SD; n, number of participants *Significant main effect of time (p

Investigation of supraspinatus muscle architecture following concentric and eccentric training.

To investigate the effects of concentric or eccentric abduction strength training on supraspinatus fiber bundle architecture and strength...
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