Effects of Open− and Closed−chainExercise of the Serratus Anterior Muscle on

Isometric Strength and Muscle ActivityRatios in Subjects With Scapular Winging

The Graduate School

Yonsei University

Department of Physical Therapy

Kiseok Nam

Effects of Open− and Closed−chainExercise of the Serratus Anterior Muscle on

Isometric Strength and Muscle ActivityRatios in Subjects With Scapular Winging

Kiseok Nam

A DissertationSubmitted to the Department of Physical Therapy

and the Graduate School of Yonsei Universityin partial fulfillment of the

requirements for the degree ofDoctor of Philosophy

June 2014

This certifies that the doctoral dissertation ofKiseok Nam is approved.

The Graduate SchoolYonsei University

June 2014

Thesis Supervisor: Ohyun Kwon

Chunghwi Yi: Thesis Committee Member #1

Hyeseon Jeon: Thesis Committee Member #2

Heonseock Cynn: Thesis Committee Member #3

Jonghyuck Weon: Thesis Committee Member #4

Acknowledgement

I sincerely thank Professor Ohyun Kwon for his excellent guidance and support to

finish my doctoral degree course. He always showed me the right way of scholarship

and facilitated my passion for learning and pride in physical therapy. I would also

deeply thank my committee, Professor Chunghwi Yi, Professor Hyeseon Jeon,

Professor Heonseock Cynn and Professor Jonghyuck Weon. Especially I also wish to

acknowledge Professor Hyukcheol Kwon who guided me in the scholar way and gave

constant encouragement.

I also express my appreciation to my friends; especially thank Jiwon Park, Yunwon

Chae and team FMT members. Also, I wish to thank sincerely my colleagues:

Professor Insul Cho, Professor Yonghyun Kwon, Professor Jongsung Chang.

Finally, I want to share this pleasure with my lovely family – Hyein Jang,

Hyeokjun Nam and Yeonu Nam. They have always gave me love and trust. Thank

you.

- i -

Table of Contents

List of Figures ···································································· iii

List of Tables ····································································· iv

Abstract ············································································ v

Chapter

I. Introduction ····································································· 1

II. Isometric Strength of the Serratus Anterior Muscle and UT/SA

and UT/LT EMG Activity Ratio in Subjects With and Without

Scapular Winging (Phase–1 study)

Method ············································································· 6

1. Subjects ······································································ 6

2. Measurement of Isometric Strength of SA muscle ······················· 9

3. EMG Recording and Data Analysis ······································· 10

4. Statistical Analysis ·························································· 12

Results ············································································ 13

III. Comparison of the Effectiveness of Open−chain and Closed−chain

Exercise of the Serratus Anterior Muscle on Isometric Strength

and Muscle Activity Ratios in Subjects Exhibiting Scapular winging

(Phase–2 study)

- ii -

Method ············································································ 18

1. Subjects ······································································ 18

2. Isometric SA Strength Measurement, EMG Recording,

and Data Analysis ···························································· 21

3. Exercise intervention ························································· 22

4. Statistical Analysis ·························································· 25

Results ············································································ 26

IV. Discussion ······································································ 31

V. Summary and Conclusion ···················································· 40

References ········································································· 42

Abstract in Korean ································································ 50

- iii -

List of Figures

Figure 1. Comparison of the isometric strength of serratus anterior

at the three scapular positions ········································· 15

Figure 2. Comparison of the EMG activity ratio of UT/SA and UT/LT ···· 17

Figure 3. Progression of closed−chain exercise ································· 23

Figure 4. Progression of open−chain exercise ··································· 24

Figure 5. Comparison of the isometric strength of serratus anterior

between pre− and post−exercise ······································ 28

Figure 6. Comparison of the EMG activity ratio of UT/SA

between pre− and post−exercise ······································ 30

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List of Tables

Table 1. Descriptive data for subjects in phase–1 study ·························· 8

Table 2. Comparison of the isometric strength of serratus anterior

at the three scapular positions ········································· 14

Table 3. Comparison of the EMG activity ratio of UT/SA and UT/LT······ 16

Table 4. Descriptive data for participants in phase–2 study··················· 20

Table 5. Comparison of the isometric strength of serratus anterior

between pre− and post−exercise······································ 27

Table 6. Comparison of the EMG activity ratio of UT/SA

between pre− and post−exercise ······································ 29

- v -

ABSTRACT

Effects of Open− and Closed−chain Exercise of the

Serratus Anterior Muscle on Isometric Strength and

Muscle Activity Ratios in Subjects

With Scapular Winging

Kiseok Nam

Dept. of Physical Therapy

The Graduate School

Yonsei University

Scapular winging (SW) is caused by weakness of the muscles that stabilize the

scapula. Dysfunction of the serratus anterior (SA) muscle triggers loss of scapular

stability during shoulder movement. Thus, strengthening of the SA is needed to

correct SW.

The general aim of the present dissertation is evaluation of the outcomes of

- vi -

strengthening exercises on SA electromyographic (EMG) activity in subjects with

and without SW. To this end, two studies were conducted.

The purpose of the phase–1 study was to compare SA isometric strength at three

different scapular positions (retracted, neutral, and protracted) and the ratios of EMG

activity between the upper trapezius and serratus anterior (UT/SA) and the upper

trapezius and lower trapezius (UT/LT) muscles in the course of isometric arm

elevation in subjects with and without SW. Thirty−three SW subjects and 33 controls

were recruited. Isometric SA strength was significantly lower in the SW group than

in controls (p < 0.05). In both groups, SA isometric strength differed significantly at

various scapular positions (p < 0.05) and was greatest in the retracted position (p

< .05). The UT/SA EMG activity ratio was significantly higher in SW subjects than

in controls (p < .005), whereas the UT/LT ratio did not differ significantly between

groups.

The phase–2 study compared the effects of open−chain exercise (OCE) and

closed−chain exercise (CCE) on SA isometric strength and on the UT/SA and UT/LT

EMG activity ratios during isometric arm elevation in SW subjects. Thirty SW

subjects were randomly placed into an OCE (three males, 12 females) or CCE group

(three males, 12 females). Mixed−model ANOVA was used to compare exercise

effects (pre−exercise vs. post−exercise) between groups (OCE vs. CCE). After

exercise, SA isometric strength increased significantly in both groups (p < 0.05) but

did not differ significantly between the groups. The UT/SA EMG activity ratio in the

post−exercise period was significantly lower than that in the pre−exercise periods in

- vii -

both the OCE and CCE groups (p < 0.05), whereas the UT/LT ratios exhibited no

significant difference.

We found that SA isometric strength was the greatest in the retracted scapular

position in both SW and non−SW subjects. The higher UT/SA EMG activity ratio in

SW subjects compared with non−SW subjects suggests that the UT muscle assumes

an important role as a scapular upward rotator during shoulder elevation in SW

subjects. The 6−week OCE and CCE interventions improved SA muscle strength

and reduced UT activity during arm elevation in SW subjects.

Key Words: Electromyography, Scapular winging, Serratus anterior, Strengthening

exercise.

- 1 -

ChapterⅠ

Introduction

Scapular winging (SW) is classically defined as a visible prominence of the

scapular medial border, as reflected in normal contact with the thoracic wall (Martin

and Fish 2008). SW represents a variant in the anatomical positioning and motion of

the scapular muscle under both static and dynamic conditions (Kibler, Wilkes, and

Sciascia 2013). Static SW is caused by either articular or bony deformities, and

dynamic SW is attributable to neuromuscular impairment. Dynamic SW is apparent in

exercise of the upper extremities accompanied by resistance (Hamano et al. 2012;

Wilk, Meister, and Andrews 2002).

Serratus anterior (SA) strength may be measured using isokinetic instruments such

as the Biodex and Cybex platforms. Commonly, SA strength measures are used to

compare variations in torque with the extent of resistance, arm elevation angle, and

shoulder position. SA strength is most commonly evaluated with the shoulder at 90°

flexion and the elbow fully extended as the subject protracts the scapula (Kendall,

Provance, and McCreary 1993).

Normal SA muscle function is essential to maintaining appropriate scapulohumeral

rhythm during arm elevation (Decker et al. 1999; Mueller et al. 2013; Wiater and

Flatow 1999; Yano 2010). SA weakness triggers changes in scapular position and thus

- 2 -

in superior elevation and medial translation; the inferior pole is also medially rotated.

Ultimately, functional scapular motion is affected. Such abnormal positioning and

movement changes the scapulohumeral rhythm of the glenohumeral joint and triggers

development of impingement syndrome (Cools et al. 2003; Ludewig and Cook 2000;

Ludewig and Reynolds 2009). SW patients present with pain, rapid fatigue, and upper

limb functional disabilities (Wiater and Flatow 1999; Kisner and Colby 2007).

Patients cannot generate muscle power, cannot elevate the arms beyond an angle of

120°, and exhibit generally unstable shoulders (Hamano et al. 2012; Ludewig et al.

2004).

Variations in muscle length and direction in the shoulder area affect intermuscular

relationships and recruitment patterns (Mottram 1997; Sahrmann 2002). Smith et al.

(2002) compared the isometric strength associated with arm elevation at three

scapular positions and found that isometric strength was reduced in the protracted

scapular position compared with the neutral position, and it was further reduced in the

retracted scapular position compared with the neutral scapular position. Garner and

Shim (2008) found that protraction force was the greatest when healthy subjects

assumed a retracted scapular position. Many studies have measured shoulder joint

strength without considering scapular positioning, and evaluations were performed at

the neutral position only (Myers et al. 2006; Wilk, Meister, and Andrews 2002). To

the best of our knowledge, no prior study has evaluated the relationship between SA

isometric strength and scapular position in those with and without SW.

In many SW studies, electromyography (EMG) has been used to measure SA

- 3 -

muscle activity, which is relevant to SW (Hardwick et al. 2006; Park et al. 2013). The

UT, LT, and SA muscles are intimately involved in upward rotation of the scapula

(Ekstrom, Donatelli, and Soderberg 2003; Ha et al. 2012). SA muscle activity

increased linearly as the arm elevation angle rose. The maximum EMG activity level

in the SA muscle was attained when subjects performed upward rotation of the

scapula with the shoulder flexed to 91％ of maximal voluntary isometric contraction

(MVIC) in the sagittal plane or abducted at 89％ MVIC in the plane of the scapula

against resistance. The activity of the LT muscle fell at angles of <90° and increased

in a log−linear manner when shoulder elevation exceeded 90°. UT muscle activity

was less than 10％ MVIC in the mid−range of shoulder elevation (from 70° to 120°),

and high−level muscle activity was apparent in the end−range of shoulder elevation

and upon shrugging movement (Moon, Kim, and Roh 2013).

Recently, workers in the field have sought to define not only EMG activity levels in

particular muscles but also interactions among the SA, UT, and LT during arm

elevation (Cools et al. 2004; Ludewig et al. 2004; Martin and Fish 2008). Sahrmann

(2002) found that abnormal movement was attributable more to among−muscle

imbalance than to muscle weakness. Ludewig and Cook (2000) proposed that a high

UT/SA activity ratio was associated with abnormal movement. Increased UT

activation with reduced activity of the LT and SA muscles during shoulder flexion

may trigger an abnormal scapulohumeral rhythm and, ultimately, SW (Cools et al.

2007; Cools et al. 2004). SW assessment features the use of EMG and isokinetic

equipment, physical examination, X−rays, MRI, and three−dimensional motion

- 4 -

analysis (3DMA). Physical examination, X−ray analysis, and 3DMA have all been

used to evaluate changes in outward scapular motion (Wang et al. 1999). These

methods measure changes in scapular angle and displacement of specific scapular

regions. Several studies of scapular movement have been performed using

radiographic procedures, but the accuracy of the data is questionable, as is the

evaluation of dynamic movement. Although many investigators claim that 3DMA is

reliable, some clinical limitations are evident. For example, it is difficult to precisely

fix markers because the relative movement of scapular bone and suprascapular skin

vary. Furthermore, these methods are too time consuming for routine clinical

application. EMG and isokinetic evaluation effectively measure muscle activity and

strength. Recently, anatomical SW changes have been evaluated by simple physical

examination using scapulometer. Weon et al. (2011) diagnosed SW by measuring the

distance between the chest wall and the inferior scapular angle; scapulometer afforded

high−level inter− and intra−test reliability.

Exercise programs for SW patients seek to strengthen the SA muscle. Recently,

diverse strengthening exercises have sought to elicit SA muscle activity to treat

shoulder dysfunction. SA exercise programs often include arm elevation, push

movements (scapular protraction), or combinations of these motions (Lombardi et al.

2008). Several exercises have been recommended to strengthen the SA and trapezius

(T) muscles based on EMG amplitudes and muscle strength.

SA strengthening exercises are principally open−chain exercise (OCE) of the

shoulder (Ha et al. 2012; Hibberd et al. 2012; Lephart and Henry 1995). Recently,

- 5 -

axial load exercises, also termed closed−chain exercise (CCE), have been developed

(Vaseghi et al. 2013). CCE is suggested to be safe and to facilitate proximal joint

stability in the early stages of rehabilitation, establishing stable upper extremity

function in both patients and healthy subjects (Lehman et al. 2006; Vaseghi et al.

2013).

The most common CCEs used to strengthen the SA muscle are push−up and

modified push−up, termed push−up plus. Choi and Lee (2013) applied push−up for 4

weeks, and reported that shoulder pain decreased and upper limb stability increased

significantly. Although the importance of pre/post evaluation of training is accepted,

few data on functional improvements after strengthening exercises have appeared. To

the best of our knowledge, no prior study has compared the effectiveness of CCE and

OCE in SW subjects.

We performed the present study in two phases. The purpose of the phase–1 study

was to compare SA isometric strength at three different scapular positions (retracted,

neutral, and protracted) between subjects with and without SW. We also compared the

UT/SA and UT/LT EMG activity ratios during isometric arm elevation in each group.

The purpose of the phase–2 study was to compare the effectiveness of OCE and CCE

in increasing isometric SA strength and to measure UT/SA and UT/LT EMG activity

ratios during isometric arm elevation in SW subjects

- 6 -

Chapter Ⅱ

Isometric Strength of the Serratus Anterior Muscle and

UT/SA and UT/LT EMG Activity Ratio in Subjects

With and Without Scapular Winging

(Phase–1 study)

Methods

1. Subjects

Sixty−six participants (16 males, 50 females) were recruited for the phase–1 study

(Table 1). We used scapulometer to identify those with and without SW. To measure

SW, each subject was asked to stand, to flex the elbow joint to 90°, and to hold the

forearm in a neutral position. A cuff weighing 5％ of body weight was attached to the

wrist (Weon et al. 2011). The examiner stood behind the subject and placed the four

pads of the scapulometer on the posterior thoracic wall in positions medial to the

vertebral border of the scapula, with the sliding board set at the level of the inferior

angle of the scapula. While holding the scapulometer in place, the examiner next

moved the sliding board anteriorly until the board touched the inferior angle of the

scapula. A ruler fixed to the board was used to measure the posterior displacement of

- 7 -

the inferior scapular angle from the thoracic wall. SW was diagnosed when the

distance between the thoracic wall and the inferior angle of the scapula was Non−SW

subjects exhibited scapulometric distances <1 cm. Weon et al. (2011) confirmed the

test–retest reliability of scapulometer for measuring SW and reported an interclass

correlation coefficient of 0.97 (95％ confidence interval: 0.87–0.99, standard error of

measurement 0.1 cm).

Participants were excluded if any of the following criteria was met: 1) limited

shoulder motion; 2) gross shoulder instability; 3) any sign or symptom of cervical

pain; 4) presence of adhesive capsulitis; 5) presence of thoracic outlet syndrome; 6)

any current complaint of numbness or tingling in an upper extremity; 7) a history of

shoulder injury or surgery; 8) participation in overhead sports at a competitive level;

and 9) upper−limb strength training for more than 5 h per week.

.

- 8 -

Table 1. Descriptive data for subjects in phase−1 study (N=66)

aMean±SD

M: male

F: female

SW: scapular winging

Parameter With SW

(n1=33, M=7, F=26)

Without SW

(n2=33, M=7, F=26)

Age (years) 26.6 ± 3.1 a

25.9 ± 2.7

Weight (㎏) 62.2 ± 4.1 64.6 ± 3.9

Height (㎝) 158.2 ± 2.8 161.2 ± 2.2

Amount of SW (㎜) 23.7 ± 1.9 7.1 ± 2.8

- 9 -

2. Measurement of Isometric Strength of the SA Muscle

SA isometric strength during scapular protraction was assessed using a Biodex

Dynamometer System 4 Pro (Biodex Medical Systems, Inc., Shirley, NY) with a

closed kinetic chain attachment. Subjects were seated upright in adjustable chairs that

accommodated subjects varying in body dimensions and were restrained using thigh,

pelvic, and trunk straps to prevent compensatory movement. A horizontal arm bar was

placed in the forward direction, and its length was adjusted to accommodate the arm

length of each subject. Prior to measurement, the arm was positioned at 90° forward

flexion of the shoulder joint with full extension of elbow joint in a thumb−up position.

During the protraction trials, SA muscle strength was measured in the retracted,

neutral, and protracted positions. The neutral position was approximately halfway

between the retracted and protracted positions. The protracted position was just short

of full protraction of the scapula, and the retracted position was just short of full

retraction. The test order was randomly selected to minimize fatigue and learning.

Isometric strength was automatically calculated by the Biodex Advantage Software

program Version 4 (Biodex, Medical Systems, Inc., Shirley, NY). Calibration of the

dynamometer was performed as described in the service manual.

- 10 -

3. EMG Recording and Data Analysis

A Noraxon TeleMyo 2400T (Noraxon TeleMyo 2400T, Noraxon, Inc., Scottsdale,

AZ) was used to measure SA, UT, and LT muscle activity. EMG electrodes were

attached to the upper and lower fibers of the T and to the SA. The latter electrodes

were placed vertically along the mid−axillary line at rib levels 6−8 (Ekstrom,

Soderberg, and Donatelli 2005). Electrodes on UT fibers were placed between a point

2 ㎝ lateral to the seventh cervical spinous process and the lateral tip of the acromion

with the shoulder held at 90° abduction. Electrodes on LT fibers were placed at

oblique vertical angles at points 5 ㎝ inferomedial from the root of the scapular

spine (Cram, Kasman, and Holtz, 1998).

Electrode sites were prepared by shaving and cleaning the skin with rubbing

alcohol (Cram, Kasman, and Holtz, 1998). Disposable silver/silver chloride surface

electrodes were positioned at inter−electrode distances of 2 ㎝. The reference

electrode was attached to the seventh cervical vertebra. Each subject was asked to

perform MVIC in test positions specific for each muscle. To measure the MVIC,

maximum SA resistance was applied to the hand and elbow with the subject in the

supine position (Ekstrom, Soderberg, and Donatelli 2005). Measurement of LT MVIC

was performed in the prone position with the shoulder externally rotated and the arm

placed overhead and parallel to the fibers of the LT while resistance was applied distal

to the elbow (Ekstrom, Soderberg, and Donatelli 2005). The UT was evaluated with

the shoulder abducted to 90° and the head in a neutral position. Downward resistance

- 11 -

was applied to the shoulder (Ekstrom, Soderberg, and Donatelli 2005).

After MVIC testing, subjects were instructed to sit on the Biodex Dynamometer

System Pro, and the arm bar was set at 120° of shoulder flexion to allow

measurement of SA, UT, and LT EMG activity during isometric upper extremity

elevation. To avoid compensatory movement, the trunk and lower extremities were

restrained with Velcro tags and belts. When the researcher gave the “Start” signal, the

subject then lifted the arm upward with maximum effort for 5 s. To prevent fatigue,

about 1 min of relaxation time was allowed between trials.

EMG signals were digitally analyzed using MyoResearch Master Edition 1.06 XP

software (Noraxon, Inc., Scottsdale, AZ). Raw analog 16−bit EMG signals were

collected at 1,000 Hz and digitized. The raw data were digitally filtered at 30~400 Hz

using a band−pass filter, and the 60 Hz signals were removed using a notch filter.

Raw data were transformed to root mean square (RMS) values to permit analysis. In

terms of normalization, each MVIC was collected over 5 s, and the mean values from

the middle 3−s epochs were averaged to obtain a final mean value. SA, UT, and LT

activity was measured during 5 s of isometric arm elevation, and the data of the

middle 3−s epochs were normalized using the 100％ MVIC method; EMG activity

ratios (UT/SA) were also calculated.

- 12 -

4. Statistical Analysis

Demographic data including gender, age, height, and weight were noted. Average

values from three trials were used in analysis. In the phase–1 study, a mixed−model

analysis of variance (ANOVA) (between: group; within: position) was used to

determine differences in SA isometric strength at 90° shoulder flexion at the three

scapular positions between those with and without SW. If a significant effect was

evident, the post−hoc Bonferroni correction was applied. Independent t−tests were

used to examine differences in UT/SA and UT/LT EMG activity ratios between the

groups. All analyses were performed using SPSS version 18.0 (SPSS, Inc., Chicago,

IL), and a p −value <0.05 was considered to reflect statistical significance.

- 13 -

Results

The SA isometric strengths at various scapular positions of subjects with and

without SW are shown in Table 3 and Figure 1. The principal effects were significant

by group (F = 9.75, p < 0.05) and position (F = 61.46, p < 0.05). No significant group

by position interaction effect was evident (F = 0.06, p = 0.92).

SA isometric strength was significantly lower in SW subjects than in controls (p <

0.05). The differences were significant at all scapular positions [retracted–protracted

(p < 0.05), protracted−neutral (p < 0.05), and neutral−retracted (p < 0.05)]. SA

isometric strength was greatest in the retracted scapular position (Table 3, Figure 1).

The UT/SA and UT/LT EMG activity ratios of subjects with and without SW are

shown in Table 4 and Figure 2. The UT/SA activity ratio in subjects with SW was

significantly higher than that in controls (p < 0.05), but the UT/LT activity ratios did

not differ significantly between the two groups (p = 0.62).

- 14 -

aMean

±S

D

UT

: up

per trap

ezius

SA

: serratus an

terior

LT

: low

er trapeziu

s

* p

<0

.05

Gro

up

Tab

le 2.

C

om

pariso

n o

f the E

MG

activity

ratio o

f UT

/SA

and U

T/L

T(u

nit: N

·m)

With

ou

t SW

With

SW

37

.11

31

.64

Retracted

Po

sition o

f Scap

ula

±

± 1

5.9

6

9.0

7a

27

.39

23

.20

Neu

tral

±

± 1

3.0

1

7.8

0

15.9

2

11.1

9

Pro

tracted

±

± 8

.25

4.1

7

9.75(0.00

*)

Group

F(p

)

61.46(0.00*)

Position

0.0

6(0

.94)

Gro

up

*P

ositio

n

- 15 -

Figure 1. Comparison of the isometric strength of serratus anterior at the three

scapular positions(mean ± SD) (*p<0.05)

- 16 -

Table3. Comparison of the EMG activity ratio of UT/SA and UT/LT

aMean±SD

SW: scapular winging

UT: upper trapezius

SA: serratus anterior

LT: lower trapezius * p<0.05

Ratio

Group

p

With SW Without SW

UT/SA 1.05 ± 0.45a 0.83 ± 0.33 0.03

*

UT/LT 1.49 ± 0.42 1.42 ± 0.62 0.62

- 17 -

Figure 2. Comparison of the EMG activity ratio of UT/SA and UT/LT

(mean ± SD) (*p<0.05)

UT/SA: ratio of upper trapezius to serratus anterior

LT/SA: ratio of lower trapezius to serratus anterior

- 18 -

Chapter Ⅲ

Comparison of the Effectiveness of Open−chain and

Closed−chain Exercise of the Serratus Anterior Muscle

on Isometric Strength and Muscle Activity Ratios in

Subjects Exhibiting Scapular Winging

(Phase–2 study)

Methods

1. Subjects

Thirty−four subjects with SW (eight males, 26 females) were initially recruited to

the phase–2 study (Table 2); these were the 26 SW subjects of the phase 1 study and

eight additional SW subjects. SW was confirmed using the procedure described above.

To reduce bias, subjects were randomly allocated to the CCE and OCE groups. Two

subjects in each group did not complete the 6−week exercise program or follow−up

testing. Fifteen subjects (three males, 12 females) in the CCE and 15 (three males, 12

females) in the OCE group completed the exercise program and all follow−up tests.

The procedure was explained in detail to all subjects, and all signed written informed

consent forms prior to the trial. The study was approved by the Yonsei University

- 19 -

Wonju Institutional Review Board in accordance with the ethical standards set by that

Board.

- 20 -

Table 4. Descriptive data for participants in phase−2 study (N=30)

aMean±SD

M: male

F: female

SW: scapular winging

Parameter Open−chain exercise

(n1=15, M=3, F=12)

Closed−chain exercise

(n2=15, M=3, F=12)

Age (years) 25.7 ± 2.7a 24.9 ± 2.1

Weight (㎏) 64.9 ± 5.2 66.7 ± 5.1

Height (㎝) 157.1 ± 3.7 160.9 ± 3.2

Amount of SW (㎜) 24.1 ± 1.4 23.3 ± 1.2

- 21 -

2. Isometric SA Strength Measurement, EMG Recording, and Data

Analysis

The instruments and experimental procedure used to measure SA strength

were the same as those of the phase–1 study. In this phase–2 study,

measurement of SA strength was performed only at the neutral scapular position.

The experimental details of EMG data recording and analysis are identical to

those of the phase–1 study.

- 22 -

3. Exercise interventions

CCE and OCE were used to strengthen the SA. A push−up plus exercise was

performed by the CCE group. Each subject placed the hands directly in front of the

shoulders with the elbows fully extended, progressed to a prone push−up using the

knees as a fulcrum, and then to a push−up while lying prone, lifting the entire body

weight (Figure 3).

Supine push−up exercises were performed by the OCE group. Each subject lay on

the floor with the shoulders flexed at 90° and the knees bent and protracted the

shoulder by pushing up a dumbbell with both hands. Resistance to protraction was

afforded initially only by the weight of the upper limb and was then increased from 1

kg to 6 kg by adding 1kg weights to the dumbbell as subjects progressed. Prior to

each exercise, the maximum distance from the table to the acromion during

protraction was noted, and subjects were verbally encouraged to maintain the

maximum protraction length during interventional exercise (Figure 4).

Each exercise was performed for 10 s and repeated 10 times per set with 7–8 sets

per day, 3 days per week over a period of 6 weeks. Resistance was progressively

increased according to individual ability. All subjects were instructed to avoid

compensatory movements. If a subject exhibited SW or continuous compensatory

movements, s/he was instructed to stop exercising, re−instructed on how the exercise

should be performed, and then asked to resume the exercise. If fatigue, pain, and

dizziness were absent, the protraction load was maximally increased.

- 23 -

Figure 3. Progression of closed−chain exercise

- 24 -

Figure 4. Progression of open−chain exercise

- 25 -

4. Statistical Analysis

Demographic data including gender, age, height, and weight were analyzed using

descriptive statistics. The averages of data from three trials were used in analysis. A

mixed−model analysis of variance (ANOVA) (between: group, within: period) was

used to explore differences in isometric SA strength pre−and post−−exercise in the

two groups. Also, a mixed−model analysis of variance (ANOVA) (between: group,

within: period) was used to evaluate pre− and post−exercise differences in UT/SA and

UT/LT EMG activity ratios between groups. All analyses were performed using SPSS

version 18.0 (SPSS, Inc.), and a p−value <0.05 indicated statistical significance.

- 26 -

Results

The isometric SA strengths of the OCE and CCE groups−by−exercise period are

shown in Table 5 and Figure 3. A significant main effect of period (F = 13.43, p <

0.05) was evident, but not of group (F = 0.86, p = 0.36). No significant

group−by−period interaction effect was noted (F = 0.04, p = 0.84). Upon post−hoc

testing, isometric strength in the post−exercise period was significantly greater than

that in the pre−exercise period in both groups (p < 0.05).

UT/SA EMG activity ratios in the two groups by exercise period are shown in

Table 6 and Figure 4. A significant main effect of period was evident (F = 18.68 p <

0.05), but not of group (F = 0.21, p = 0.65). No significant group−by−period

interaction effect (F = 0.07, p = 0.79) was noted. Upon post−hoc testing, the activity

ratios in the post−exercise period were significantly lower than those in the

pre−exercise period in both groups (both p−values <0.05).

The UT/LT EMG activity ratios in the two groups by exercise period showed no

significant main effect of period (F = 3.31, p = 0.08) or group (F = 0.02, p = 0.89).

No significant group−by−period interaction effect was evident (F = 1.72, p = 0.20).

- 27 -

Table 5. Comparison of the isometric strength of serratus anterior between pre− and

post−exercise (unit: N·m)

aMean±SD

CCE: closed−chain exercise

OCE: open−chain exercise * p<0.05

Group Period F(p)

Pre−Exercise Post−Exercise Group Period Group*Period

CCE 9.47 ± 3.40a 23.79 ± 18.26 0.86(0.36) 13.43(0.00

*) 0.04(0.84)

OCE 12.91 ± 4.26 28.92 ± 28.15

- 28 -

Figure 5. Comparison of the isometric strength of serratus anterior between pre− and

post−exercise

- 29 -

Table 6. Comparison of the EMG activity ratio of UT/SA between pre− and

post−exercise

aMean±SD

CCE: closed−chain exercise

OCE: open−chain exercise * p<0.05

Group Period F(p)

Pre−Exercise Post−Exercise Group Period Group*Period

CCE 0.91 ± 0.22a 0.69 ± 0.26 0.21(0.65) 18.68(0.00

*) 0.07(0.79)

OCE 0.93 ± 0.10 0.74 ± 0.30

- 30 -

Figure 6. Comparison of the EMG activity ratio of UT/SA between pre− and

post−exercise

- 31 -

Chapter Ⅳ

Discussion

The purpose of the phase–1 study was to compare SA isometric strengths at three

different scapular positions (retracted, neutral, and protracted) between subjects with

and without SW. We also compared UT/SA and UT/LT EMG activity ratios during

isometric arm elevation in both groups.

Uniquely, we measured SA isometric strengths at different scapular positions in

subjects with and without SW. Previous studies measured the strengths of the SA and

shoulder girdle muscles employing various maneuvers, but scapular position was not

considered, and all subjects were healthy (Cools et al. 2002; Garner and Shim 2008;

Smith et al. 2002; Wang, Normile, and Lawshe 2006). Cools et al. (2002) measured

unilateral isokinetic protraction strength in healthy subjects. Scapular position was not

considered when measuring SA strength in the scapular plane. Although Garner and

Shim (2008) measured bilateral isometric protraction strength at three scapular

positions (retracted, neutral, and protracted), all subjects were healthy. The cited

authors found that protraction force was strongest in the retracted scapular position, as

did we. The peak protraction force in the protracted position (951 N) was 85％ of

that in the retracted position (1,117 N). We found that the isometric strength of the SA

in the protracted position was 35％ and 42％ that of the retracted position in SW

- 32 -

subjects and controls, respectively. The difference between these values and those of

Garner and Shim (2008) may be explained by the fact that those authors measured

bilateral protraction strength in healthy subjects, whereas we measured unilateral

protraction strength in subjects with and without SW.

The ability of a muscle to generate force depends on the length to which the muscle

is extended when delivering the maximum force; this is usually close to the normal

resting length in the mid−range of motion. However, our findings and those of

previous studies (Garner and Shim 2008) found that SA strength was greatest in the

retracted scapular position, when the SA is maximally extended. The relationship

between muscle strength and length is termed the length−tension relationship.

Muscles that tend to be long, such as the SA, the gluteus medius, and the gluteus

maximus, can generate substantial tension at appropriate points, affording positional

strength (Carrie, and Lori 2005). The positional strength of the SA is maximal at the

retracted scapular position. This muscle generates maximal tension when it is fully

extended and the least tension when it is contracted. When a lengthened muscle is

shortened, myofilaments overlap excessively and cannot develop maximal tension

(Sahrmann 2002). Therefore, an SA strength test should be performed at multiple

points in the extension range to determine whether the SA is positionally weak at any

point in that range (Carrie and Lori 2005).

In the present study, we measured SA strength at 90° forward flexion of the

shoulder joint, full extension of the elbow joint, and in the thumb−up position. Wang

et al. (2006) and Garner and Shim (2008) employed the same posture. Methods for

- 33 -

measuring SA strength have been described in several studies and include protraction

in the scapular plane, protraction when the shoulder is flexed at 90° in the sagittal

plane, and protraction at 90° shoulder flexion and 105° horizontal adduction of the

shoulder joint (Cools et al. 2002; Garner and Shim 2008; Wang et al. 2006). Of these

positions, shoulder protraction at 90° is most commonly applied during measurement

of SA strength. We used this method. The other methods may be effective, but they

are not recommended because other muscles are activated as agonists during arm

elevation. Thus, it is difficult to focus solely on the SA muscle using such methods.

The EMG activity of the SA, UT, and LT was measured, and we calculated the

UT/SA and UT/LT activity ratios. Previous studies found that the UT, LT, and SA

muscles acted agonistically during scapular movement with arm elevation and were

the only muscles involved in upward rotation of the scapula (John and Paula 2001).

The SA muscle generates resistance during upward rotation of the scapula with the

shoulder flexed. LT muscle activity falls when shoulder flexion is below 90° and

progressively increases as that angle rises. UT muscle activity is less than 10％ of

maximal in the mid−range of shoulder elevation, becoming higher in the end range

(Moon, Kim, and Roh 2013). Furthermore, abnormal movements were associated

with muscle imbalance to a greater extent than muscle weakness was (Sahrmann

2002). Ludwig and Cook (2000) showed that a high UT/SA ratio contributed to

abnormal movement during shoulder elevation. Thus, increased UT activation may

trigger an abnormal scapulohumeral rhythm and, ultimately, SW. Reduced activity of

- 34 -

the SA and LT muscles during shoulder flexion is also believed to trigger abnormal

scapular movement (Cools et al. 2004; Cools et al. 2007). If the SA muscle does not

adequately rotate the scapula upward, activation of the UT muscle may increase,

stressing the acromioclavicular joint (Johnson et al. 1994). Poor control of the scapula

by the SA muscle can create stress at the glenohumeral joint (Sahrmann 2002).

The UT/SA EMG activity ratios differed significantly between groups. Thus, UT

muscle activity in the SW group was significantly higher than that in controls. Our

results are similar to those of previous studies. Huang et al. (2013) compared UT/SA

activation ratios during forward flexion in subjects with and without impingement

syndrome by contraction type (concentric, eccentric, and isometric contraction) and

found that the UT/SA ratio during isometric shoulder−forward flexion was almost 0.6

in normal subjects but 0.7–0.8 in those with impingement syndrome. Other studies

have yielded slightly different results. Martin et al. (2008) and Ludewig et al. (2004)

calculated ratios of almost 0.3 when subjects maintained the push−up plus posture on

both stable and unstable surfaces. Pirauá et al. (2014) calculated UT/SA muscle

activation ratios of 0.5–1 using electrodes attached to the SA muscle; the results

varied with exercise surface (stable or unstable) when SW subjects performed

push−up exercises. Differences in UT/SA ratios may be explained by variation in

exercise methods, the type of contraction measured, and the sites of electrode

placement on the SA muscle. Thus, higher UT activation reflects abnormal scapular

motion caused by a weakened SA. Specifically, when movements are performed over

the same range of motion, decreased activity in one muscle may be associated with

- 35 -

increased activity in another to achieve the same range of motion (Oh et al. 2007).

Page et al. (2010) found that muscles act synergistically. It was also reported that

reduced SA activation in subjects with shoulder pain triggered increased

compensatory UT muscle activity (Martin and Fish 2008). Thus, the UT/SA activity

ratio was significantly higher in SW patients.

The phase–2 study uniquely revealed that both OCE and CCE improved isometric

SA strength and UT/SA and UT/LT EMG activity ratios. To the best of our knowledge,

this is the first study to identify the utility of SA strengthening exercises during arm

elevation in SW subjects. No prior study has compared the effectiveness of OCE and

CCE used to strengthen the SA and improve the UT/SA ratio in subjects with SW.

CCE was the push−up plus exercise, performed in the prone position with the knees

on the floor and the shoulder protracted. OCE was applied in the supine position with

the shoulder protracted vertically upward and using hand−held dumbbells. In

previous work, CCE−mediated SA strengthening usually entailed push−up plus

exercises and modifications thereof. The SA muscle exhibited relatively high−level

activity, and the UT/SA ratio was low in the plus phase of this exercise (Huang et al.

2013; Kim 2014; Ludewig 2004; Pirauá 2014). Especially, the kneeling push−up plus

exercise is considered optimal for SA training based on the low UT/SA ratio achieved

(Huang et al. 2013). The CCE method we used was a knee push−up plus exercise,

similar to that of previous studies.

In previous studies, various OCEs have been used to strengthen the SA, including

the dynamic hug exercise, shoulder protraction, scaption, and wall−slide exercise with

- 36 -

resistance provided by body weight, an elastic band, or dumbbells (Decker et al. 1999;

Hardwick 2006). Of these methods, shoulder protraction using dumbbells or elastic

bands has most commonly been used to strengthen the SA. Therefore, we used

protraction with dumbbells in the present study

The effects of CCE and OCE were compared in terms of improvements in SA

isometric strength and UT/SA and UT/LT EMG activity ratios in subjects with SW.

The SA isometric strength increased significantly after exercise in both groups, and

no between group difference was evident. Also, the UT/SA EMG activity ratio

decreased significantly after exercise in both groups; again, no between−group

difference was evident. These findings suggest that both OCE and CCE improve SA

isometric strength in individuals with SW. Our current study revealed that SA

isometric strength improved by 150.26％ after CCE and 124.01％ after OCE; the

between group difference was not significant. The utility of CCE and OCE as SA

strengthening exercises for SW subjects has not been previously evaluated. Earlier

work sought to strengthen shoulder muscles in subjects with subacromial

impingement syndrome and in college−level and adolescent swimmers (Başkurt et al.

2011; Hibberd et al. 2012; Van de Velde et al. 2011). Başkurt et al. (2011) found that

scapular stabilization exercises improved SA strength from 8.79 kg before treatment

to 10.19 kg and increased SA strength by 15.9％ in patients with subacromial

impingement syndrome. Hibberd et al. (2012) found that a 6−week strengthening

program directed toward stabilization of the shoulder and scapula did not improve

- 37 -

muscle strength or kinematic scapular parameters in college−level swimmers. Van de

Velde et al. (2011) found that a 12−week scapula training program improved the peak

protraction force in the dominant (13.7％) and nondominant sides (12.5％) compared

with pre−training values.

Ellenbecker and Davies (2001) developed a CCE that was effective for stabilizing

scapular synergy and the SA. Additionally, the exercise stabilized the shoulder when

the distal region of the upper limb was fixed, and facilitated proprioception by

redistributing pressure in the joint capsule (Iwasaki and Matsuse 2006). Antagonist

muscles were eccentrically co−activated with agonist muscles, increasing the stability

of injured joints (Iwasaki and Matsuse 2006). However, our findings differed,

although the maneuver used to measure SA isometric strength was similar to OCE. It

is generally true that the effects of training are most evident when the same exercise

type is used for both training and testing (Carrie and Lori 2005), and the training

mode chosen (OCE or CCE) influences the effectiveness of training (Timothy, Bruce,

and John 2009). The posture we chose for isometric SA strength measurement was

similar to the OCE position. Thus, the reason that our findings differ from those of

previous studies may be that the strengthening and testing modes differed in for CCE

but for OCE.

The UT/SA EMG activity ratio decreased significantly after OCE and CCE in the

present study. Recent work with SW subjects has treated the shoulder dysfunction by

using selective strengthening exercises to facilitate SA muscle activity (Kiss, Illyes,

- 38 -

and Kiss 2010; Neumann 2002). Additionally, many previous studies found that

strengthening regimens including push−up and push−up plus exercises increased

EMG activity of the SA muscle and rehabilitated the upper limbs (Hardwick et al.

2006). Other studies yielded similar results (Huang et al. 2013; Pirauá et al. 2014).

The UT/SA EMG activity ratio of SW subjects during push−up plus exercise on

stable and unstable surfaces were 0.52 and 0.87, respectively. The UT/SA ratio was

0.61 in normal adults and 0.70 in an impingement group during isometric

shoulder−forward flexion (Huang et al. 2013), in line with our finding that the UT/SA

ratio was higher in the SW group than in controls, with values of 1.05 and 0.83,

respectively.

Excessive UT activation is associated with abnormal kinematics of the shoulder

girdle and develops to compensate for reduced SA activity (Ludewig and Cook 2000).

Thus, we believe that the lower UT/SA ratio may be associated with increased SA

strength and reduced UT activation.

Both OCE and CCE improved isometric SA strength and the UT/SA EMG activity

ratio. Thus, both exercises correct imbalances in synergistic muscle activities during

upward scapular rotation.

However, our study had some limitations. Muscles including the pectoralis major,

pectoralis minor, and rhomboid, which could affect scapular movement, were not

considered. Furthermore, follow−up testing to evaluate the lasting nature of the

intervention was not performed. Despite these limitations, we provide useful clinical

evidence on the effectiveness of strengthening exercises in SW subjects. Further

- 39 -

studies lacking the above limitations are needed to gather more detailed evidence.

- 40 -

Chapter Ⅴ

Summary and Conclusion

In our phase–1 study, we compared SA isometric strengths at three different

scapular positions (retracted, neutral, and protracted) and the UT/SA and UT/LT

EMG activity ratios during isometric arm elevation in subjects with and without SW.

SA isometric strength was significantly lower in SW subjects compared with

controls. SA isometric strengths differed significantly between groups in the

retracted, neutral, and protracted scapular positions. SA isometric strength was

greatest in the retracted scapular position. Also, the UT/SA EMG activity ratio was

significantly higher in SW subjects than in controls, whereas the UT/LT ratios did

not differ significantly between groups.

In our phase–2 study, we compared the effectiveness of 6−week OCE and CCE SA

muscle therapy on SA isometric strength and the EMG activity ratios (UT/SA and

UT/LT) during isometric arm elevation in SW subjects. After exercise, the isometric

SA strength increased significantly in both groups and did not differ significantly

between groups. The UT/SA EMG activity ratios in the post−exercise period were

significantly lower than those in the pre−exercise period in both the OCE and CCE

groups, but the pre− and post−exercise UT/LT ratios did not differ significantly

between groups.

SA isometric strength was greatest in the retracted scapular position in subjects

- 41 -

with and those without SW. The higher UT/SA EMG activity ratio in SW subjects

compared with non−SW subjects suggests that the UT assumed a dominant role

among the upward scapular rotators during shoulder elevation in SW subjects.

Following 6−week OCE and CCE intervention, the strength of the SA muscle during

arm elevation increased, and that of the UT fell in SW subjects.

- 42 -

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2010;19(2):209-215.

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국문 요약

날개어깨뼈 대상자를 위한 앞톱니근 열린사슬운동과

닫힌사슬운동이 앞톱니근의 등척성 근력과

근활성도 비에 미치는 영향

연세대학교 대학원

물리치료학과

남기석

날개어깨뼈는 앞톱니근, 위등세모근, 아래등세모근과 같은 어깨뼈 안정

화 근육의 불균형으로 발생한다. 앞톱니근의 기능부전은 어깨의 움직임 동

안 어깨뼈의 안정화 소실을 초래한다. 그러므로 앞톱니근의 강화운동은 날

개어깨뼈의 치료를 위해 거론된다.

1단계 연구는 날개어깨뼈가 있는 대상자와 없는 대상자간에 어깨관절의

등척 굽힘 동안 앞톱니근의 등척성 근력을 세 개의 어깨뼈 위치(들임위치,

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중립위치, 내밈위치)에서 비교하고, 위등세모근에 대한 앞톱니근의 근전도

활성비율 및 위등세모근에 대한 아래등세모근의 근전도 활성비율을 비교하

기 위하여 날개어깨뼈가 있는 대상자 33명과 날개어깨뼈가 없는 33명을

대상으로 하였다. 두 그룹간에 세 가지의 어깨뼈 위치에 따른 앞톱니근의

등척성 근력을 비교하기 위하여 혼합모형 분산분석 (mixed-model

ANOVA)을 실시하였으며, 근전도 활성비율을 비교하기 위하여 독립표본

t-검증을 실시하였다. 앞톱니근의 등척성 근력은 날개어깨뼈가 있는 그룹

이 없는 그룹에 비해 근력이 유의하게 약한 것으로 나타났다 (p<.05). 세

가지의 어깨뼈 위치에 따른 앞톱니근의 등척성 근력의 비교에서 날개어깨

뼈가 있는 그룹과 없는 그룹 모두에서 유의한 차이가 있었다 (들임위치-

내밈위치(p<.05), 내밈위치-중립위치 (p<.05), 중립위치-들임위치

(p<.05)). 어깨뼈 들임위치에서의 앞톱니근의 등척성 근력이 내밈위치와

중립위치에 비해서 유의하게 강하였다 (p<.05). 위등세모근에 대한 앞톱니

근의 근전도 활성비율은 날개어깨뼈가 있는 그룹이 없는 그룹에 비해 유의

하게 높았으며, 위등세모근에 대한 아래등세모근의 근전도 활성비율은 두

그룹간에 차이가 없었다 (p<.05).

2단계 연구는 날개어깨뼈가 있는 대상자에게 6주간의 열린사슬운동과

닫힌사슬운동을 적용하여 어깨관절 등척성 굽힘 동안 앞톱니근의 등척성

근력과 위등세모근에 대한 앞톱니근의 근전도 활성비율 및 위등세모근에

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대한 아래등세모근의 근전도 활성비율에 미치는 영향을 비교하기 위하여

실시하였다. 날개어깨뼈가 있는 30명을 열린사슬운동 그룹 (남자 3명, 여

자 12명)과 닫힌사슬운동 그룹 (남자 3명, 여자 12명)에 무작위 배정하였

다. 열린사슬운동 그룹과 닫힌사슬운동 그룹간 운동전후의 앞톱니근 등척

성 근력과 근전도 활성비율을 비교하기 위하여 혼합모형 분산분석

(mixed-model ANOVA)을 실시하였다. 두 그룹 모두에서 운동 후에 앞

톱니근의 등척성 근력이 유의하게 증가하였으며 (p<.05), 두 그룹간에는

유의한 차이가 없었다. 위등세모근에 대한 앞톱니근의근전도 활성비율은

열린운동사슬 그룹 (p<.05)과 닫힌사슬운동 그룹 (p<.05) 모두에서 운동

전에 비해 운동 후에 유의하게 감소하였다. 그러나 위등세모근에 대한 아

래등세모근의 근전도 활성비율은 두 그룹 모두에서 운동 전과 운동 후에

유의한 차이가 없었다.

이 연구의 결과를 요약하면 날개어깨뼈가 있는 대상자와 없는 대상자 모

두에서 어깨뼈 들임 자세에서 앞톱니근의 등척성 근력이 내밈자세와 중립

위치에 비해 유의하게 강하였다. 날개어깨뼈가 있는 대상자는 없는 대상자

에 비해 위등세모근에 대한 앞톱니근의 근전도 활성비율이 높았는데 이 결

과는 날개어깨뼈가 있는 대상자가 팔을 들어올리는 동안 어깨뼈 위쪽 돌림

근 중에서 위등세모근이 우세하게 사용한다는 것을 의미한다. 그리고 날개

어깨뼈 대상자에게 적용한 6주간의 열린 사슬운동과 닫힌 사슬운동은 두

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운동방법 모두 앞톱니근의 등척성 근력을 향상시키고, 팔을 위로 들어올리

는 동작 동안 위등세모근의 활성도를 감소시키는데 효과적일 것으로 사료

된다.

핵심 되는 말: 강화운동, 근전도, 날개어깨뼈, 앞톱니근.