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Journal of Back and Musculoskeletal Rehabilitation 00 (2014) 1–6 1

DOI 10.3233/BMR-140458
IOS Press

Activation of the serratus anterior and upper

trapezius in a population with winged and
tipped scapulae during push-up-plus and
diagonal shoulder-elevation
Se-Yeon Parka and Won-Gyu Yoob,∗
a
Department of Physical Therapy, The Graduate School, Inje University, Gyeongsangnam-do, Korea
b
Department of Physical Therapy, College of Biomedical Science and Engineering, Inje University,
Gyeongsangnam-do, Korea

Abstract.
OBJECTIVES: Scapular winging and tipping are types of abnormal scapular kinematics, which is caused by not only the en-
trapment of peripheral nerve, but also imbalance of the scapulothoracic musculatures. The purpose of this study was to investi-
gate the presence of muscular imbalance in the middle and lower parts of the serratus anterior and upper trapezius in people with
scapular winging and tipping.
METHODS: 20 male participants (age, 23.0 ± 1.92 y) were placed into symptomatic group (n = 10) and control group (n =
10). Participants completed two individual trials of a push-up plus, and a diagonal shoulder elevation, while electromyography
(EMG) recorded muscle activity of the low and middle serratus anterior and upper trapezius. The root mean squared EMG values
for three muscles were normalized using maximum voluntary isometric contractions (%MVIC). The value was calculated using
modified isolation equation for comparing activation of middle and lower serratus anterior (%isolation).
RESULTS: During a diagonal shoulder elevation, the % maximal voluntary isometric contraction (%MVIC) data showed that
the symptomatic participants had significantly greater activation of the middle serratus anterior compared to the control group
(P = 0.01). During a diagonal shoulder elevation, the symptomatic participants had not only significantly increased %isolation
of the middle serratus anterior, but also significantly decreased for the lower serratus anterior compare with the control group
(p = 0.00).
CONCLUSION: Present result indicated that different muscle activation between middle and lower serratus anterior could rep-
resent in group with scapular dyskinesis, and need for selective activation of the lower serratus anterior in patients with scapular
winging and tipping.

Keywords: Electromyography, scapular winging, scapular tipping, shoulder rehabilitation, scapular dyskentsis test

1 1. Introduction and dorsal scapular nerves, which innervate the ser- 4

ratus anterior, trapezius, and rhomboid muscles, re- 5

2 Abnormal scapular orientation such as winging is spectively [1]. Injuries causing scapular winging are 6

3 caused by lesions of the long thoracic, accessory, rare and may require surgical management in some 7

cases [1]. It has been also suggested that postural 8

changes due to muscle imbalance could result in wing- 9

∗ Corresponding author: Won-Gyu Yoo, Department of Physical ing of the scapula [2]. The serratus anterior positions 10
Therapy, College of Biomedical Science and Engineering, Inje Uni-
versity, 607 Obangdong, Gimhae, Gyeongsangnam-do 621 749, Ko-
the scapula closely against the thorax and confers sta- 11

rea. Tel.: +82 55 320 3994; Fax: +82 55 329 1678; E-mail: won7y@ bility to the scapula, which prevents the medial border 12

inje.ac.kr. or inferior angle of the scapula from projecting posteri- 13

c 2014 – IOS Press and the authors. All rights reserved

ISSN 1053-8127/14/$27.50 ⃝
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2 S.-Y. Park and W.-G. Yoo / Effect of scapular dykinesis on exercises

Table 1
Averaged participant’s demographic data
anterior and the upper trapezius during a push up plus 58

and diagonal shoulder elevation in individuals with and 59

Control group Symptomatic group
without scapular dyskinesis. 60
Age (year) 23.9 ± 1.79 22.1 ± 1.66
Height (Cm) 173.58 ± 3.65 176.70 ± 3.74
Weight (kg) 67.30 ± 4.72 68.40 ± 6.15
BMI (Kg/m2 ) 22.48 ± 1.32 22.67 ± 1.98 2. Methods 61

2.1. Participants 62
14 orly [3,4]. Therefore, weakness of the serratus anterior
15 could contribute to altered scapular kinematics such as The study was approved by the Inje University Fac- 63
16 winging and tipping. ulty of Health Science Human Ethics Committee, and 64

17 Sahrmann [5] stated that an increased activation of all participants provided written informed consent be- 65

18 upper trapezius was necessary for compensating weak- fore starting the study. This study enrolled 20 male 66

19 ness of serratus anterior. General function of the up- participants (age 23.0 ± 1.92 years, height 175.14 ± 67

20 per trapezius includes upward rotation and elevation 3.94 cm, weight 67.85 ± 5.36 kg, and body mass in- 68

21 of scapula, which have been also regarded as a scapu- dex 22.12 ± 1.59). The demographics of each group 69

22 lar stabilizer. However, Ludewig et al. [6,7] suggested are summarized in Table 1. The participants had no 70

23 that excessive activation of upper trapezius should be history of musculoskeletal disorders or pain associ- 71

24 avoided because the kinematic contribution of the up- ated with the upper extremity in the past six months. 72

25 per trpaeizus to the upward rotation of the scapulotho- Three physical therapists evaluated the participants for 73

26 riacic movement is less than that of the serratus ante- the presence or absence of scapular dyskinesis. All of 74

27 rior. In previous researches, upper trapezius and serra- the participants were asked to elevate their arms over- 75

28 tus anterior were compared using its ratio for evaluat- head within three seconds in a thumbs-up position, 76

29 ing effectiveness of exercises [6,8]. and lower them within three seconds. A cuff formed 77

30 Some exercises were recommended for activat- load was attached to the participant’s forearm accord- 78

31 ing serratus anterior selectively which were including ing to the participant’s weight: 3 lb for those weighing 79

32 push-up plus, diagonal shoulder flexion, dynamic hug, less than 68.1 kg and 5 lb for those weighing 68.1 kg 80

or more. The participants performed four repetitions 81

33 serratus anterior punch, and wall slide tasks [6–12]. It
(two for flexion and two for abduction), which were 82
34 was suggested that the push-up plus task activates the
recorded by a video camera. Three physical therapists 83
35 middle parts of serratus anterior selectively, minimiz-
determined the presence of scapular dyskinesis by con- 84
36 ing activation of the upper trapezius [6,11]. Ekström
sensus [13]. To exclude the participants with impinge- 85
37 et al. [9] reported that diagonal shoulder elevation ac- ment syndrome, Neer impingement test (presence of 86
38 tivated the lower parts of serratus anterior the greatest pain with passively flexed shoulder at end range) and 87
39 compared to several other exercises in their study. Hawkins-Kennedy test (presence of pain with passive 88
40 Regarding abnormal kinematics of the scapula, in- internal rotation in position of 90◦ shoulder flexion and 89
41 cluding winging, tipping, and excessive elevation, Mc- the 90◦ elbow flexion) were also conducted by the ther- 90
42 Clure et al. [13] proposed the scapular dyskinesis test apists. 91
43 for determining abnormal scapular kinematics with the
44 researcher observing from behind while the partici- 2.2. Measuring instrument 92

45 pant performed a dynamic load task. Although scapu-

46 lar dyskinesis test has been evaluated reliability and To measure middle and lower serratus anterior re- 93

47 validity through altered scapular kinematics using a cruitment, the surface electromyography (sEMG) sig- 94

48 three-dimensional motion-capturing system [14], there nal was amplified, band-pass filtered (20–450 Hz), and 95

49 was no report that this symptom is directly associated then collected using a Trigno wireless system (DelSys, 96

50 with specific impairment of serratus anterior or altered Boston, MA, USA). The sEMG was recorded digitally 97

at 2000 Hz/s, and the root mean square (RMS) was cal- 98
51 activation of upper trapezius.
culated with EMG Works 4.0 analysis software (Del- 99
52 In this study, we hypothesized that participants with
Sys, Boston, MA, USA). 100
53 scapular winging and tipping have weakness in parts
54 of the serratus anterior and that there is greater acti- 2.3. Procedure 101
55 vation of the upper trapezius in the group with abnor-
56 mal scapular kinematics. Purpose of present study was Wireless surface electrodes (DelSys, Boston, MA, 102

57 to investigate the activation of the parts of the serratus USA) were attached parallelto the muscle fibers on the 103
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S.-Y. Park and W.-G. Yoo / Effect of scapular dykinesis on exercises 3

Fig. 1. Demostration of the diagonal elevation and push-up plus. A: Diagonal elevation, B: Push up plus.

104 right side as follows: on the middle serratus anterior rax in a weight-bearing posture. The initial posture 139

105 (MSA) at approximately the mid-axillary line on the was a quadruped posture with the knees extended 140

106 right side over the fifth rib, on the lower serratus ante- and the distance between the hands and feet equal to 141

107 rior (LSA) on the belly of the muscle where it branches 75% of the participant’s height [19]. Included exer- 142

108 to the seventh rib, and on the upper trapezius (UT) cises were demonstrated in Fig. 1. Each task was per- 143

109 approximately half the distance between the seventh formed within 3 seconds and was controlled by a 60- 144

110 cervical spinal process and the acromion [11,15]. Be- Hz metronome. Every participant performed the two 145

111 fore attaching the electrodes, the skin was cleaned with tasks twice in a randomized order and took a 1-minute 146

112 snap paper and alcohol. To confirm the electrode at- rest between trials. 147

113 tachment at the serratus anterior, each rib level was

114 marked with tape to the tenth rib, which could be pal- 2.4. Statistical analysis 148

115 pated as the end of the false rib.

116 For each muscle, the maximum voluntary isomet- The raw EMG data were full-wave rectified and in- 149

117 ric contraction (MVIC) was measured to normalize tegrated over the 3-second period of each exercise. The 150

118 the sEMG amplitude during the diagonal shoulder- mean integrated EMG value of two trials for each con- 151

119 elevation and push-up-plus tasks. Following a previ- dition was used for subsequent statistical analyses and 152

120 ous study that investigated normalization of the serra- is expressed as a percentage of the maximum voluntary 153

121 tus anterior and upper trapezius activity, two trials of isometric contraction (%MVIC) values normalized rel- 154

122 MVIC were performed while applying manual resis- ative to the MVIC. To analyze the intramuscular re- 155

123 tance during (1) scapular protraction with the shoulder sponse of the serratus anterior to exercise, the mean 156

124 flexed at 90◦ within supine position, (2) upward scapu- integrated EMG value recorded from each part of the 157

125 lar rotation with the shoulder flexed at 125◦ within serratus anterior relative to the mean EMG activation 158

126 sitting position, (3) upward scapular rotation with the recorded from the middle and lower fibers of the serra- 159

127 shoulder flexed in the scaption plane (almost 35◦ ante- tus anterior muscles was calculated using the modified 160

128 rior to the frontal plane) at 125◦ within sitting [16]. Af- isolation equation. 161

ter measuring the MVIC, each participant performed ! "

129
EMGxvi
130 the push-up plus and diagonal shoulder elevation above Isolationxvi (%) = ∗100
EMGMSAvi + EMGLSAvi
131 90◦ with a load.
132 The loaded shoulder-elevation was performed in the Where x represents the muscle in each calculation, and 162

133 sitting position, and the load was determined as the y and i indicate the specific exercise and trial, respec- 163

134 five-repetition maximum (5RM) lifting capacity for tively. If the middle part of the serratus anterior was not 164

135 each participant [9]. The load for 5RM and height active during a certain exercise, then the percent isola- 165

136 of the participants were determined before the day of tion of the lower part of the serratus anterior was 100% 166

137 the experiment. The push-up plus exercise was con- for that exercise. In previous research conducted by Ar- 167

138 sidered full protraction of the scapula against the tho- lotta et al. [17], this equation was used to investigate 168
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4 S.-Y. Park and W.-G. Yoo / Effect of scapular dykinesis on exercises

Table 2
Descriptive statistics of normalized EMG data (%MVICRMS ) of the three muscles during push-up plus and diagonal shoulder elevation
Muscles %MVIC
Diagonal shoulder elevation Push up plus
Control Symptomatic t-value p-value Control Symptomatic t-value p-value
MSA 59.95 ± 23.66 102.18 ± 42.47 −2.74* 0.01* 74.96 ± 21.78 75.57 ± 33.50 −0.04 0.96
LSA 89.82 ± 25.37 78.23 ± 24.44 1.04 0.31 75.67 ± 23.39 80.46 ± 32.05 −0.38 0.70
UT 64.90 ± 25 51.68 ± 16.93 1.38 0.18 7.97 ± 3.54 7.52 ± 4.35 0.25 0.80
*p < 0.05. MVIC: Maximum voluntary isometric contraction, MSA: Middle serratus anterior, LSA: Lower serratus anterior, UT: Upper trapezius.

Table 3
Descriptive statistics of calculated EMG data (%isolation) in middle and lower serratus anterior during push-up plus and diagonal shoulder
elevation
Muscles %isolation
Diagonal shoulder elevation Push up plus
Control Symptomatic t-value p-value Control Symptomatic t-value p-value
MSA 33.20 ± 9.43 55.49 ± 6.71 −6.09* 0.00* 42.68 ± 6.03 48.31 ± 11.75 −1.34 0.19
LSA 66.79 ± 9.43 44.50 ± 6.71 6.09* 0.00* 57.31 ± 6.03 51.68 ± 11.75 1.34 0.19
*p < 0.05. MSA: Middle serratus anterior, LSA: Lower serratus anterior.

169 selective exercises for the lower trapezius in compari- in the symptomatic participants, whereas the symp- 199

170 son with other parts of the trapezius. The SPSS statis- tomatic participants had significantly lower %isolation 200

171 tical package (version 12.0; SPSS, Chicago, IL, USA) values for the lower serratus anterior. No significant 201

172 was used to analyze the significance of differences be- differences in the %isolation were found for both the 202

173 tween two groups in terms of the activation of the mid- middle and lower serratus anterior during the push-up- 203

174 dle serratus anterior, lower serratus anterior, and up- plus task (Table 3). 204

175 per trapezius during the push-up-plus and loaded diag-

176 onal shoulder-elevation tasks. The two-tailed indepen-
177 dent t-test was used to determine the differences in the 4. Discussion 205

178 %MVIC and %isolation between groups. The level of

This study examined participants with and without 206
179 significance was p < 0.05. The results were expressed
scapular winging and tipping. Although the partici- 207
180 as mean ± standard deviation for each group.
pants had scapular dyskinesis with scapular winging or 208

tipping while elevating or lowering the arm, they did 209

not have severe pain or functional limitation in daily 210

181 3. Results
life. Madeson et al. [18] reported that the prevalence of 211

scapular dyskinesis increased with cumulative swim- 212

182 A significant difference in the %MVIC of the mid- ming training in a pain-free population, which indi- 213
183 dle serratus anterior between the symptomatic and con- cates that scapular dyskinesis can appear in a pain- 214
184 trol groups was observed during the diagonal shoulder- free population and may be caused by low muscular 215
185 elevation. For diagonal shoulder elevation, the symp- endurance. Although scapular dyskinesis can occur in 216
186 tomatic participants had significantly greater %MVIC a pain-free population, the scapular kinematics of the 217
187 of the middle serratus anterior compared with the con- dyskinesis is reported to be similar to that of partic- 218
188 trol group (Table 2). The average %MVIC of the lower ipants with impingement syndrome [13]. Therefore, 219
189 serratus anterior was lower in the symptomatic partici- scapular dyskinesis could be interpreted as a risk factor 220
190 pants than in the controls, although the difference was for shoulder disorders. The EMG values were analyzed 221
191 not significant. For the upper trapezius, the %MVIC using normalization and isolation. In the normalization 222

192 did not differ between the two groups for the diago- method, we determined the MVIC for the upper trapez- 223

193 nal shoulder-elevation and push-up-plus tasks. For the ius and serratus anterior several ways because of the 224

194 push-up plus task, there was no significant difference presence of methodological and individual differences 225

195 in the %MVIC of the middle and lower serratus ante- in measurement of the MVICs [16]. 226

196 rior (Table 2). During the push-up-plus task, the %MVIC and 227

197 During diagonal shoulder elevation, the %isolation %isolation of the muscles studied did not differ signifi- 228

198 of the middle serratus anterior was significantly higher cantly between the two groups, consistent withprevious 229
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S.-Y. Park and W.-G. Yoo / Effect of scapular dykinesis on exercises 5

230 work. Although the participants had different symp- part, which might represent excessive anterior tilt (tip- 281

231 toms, Ludewig et al. [6] also reported no significant ping) and excessive internal rotation (winging) of the 282

232 difference in activation of the serratus anterior between scapula. Lin et al. [23] found that the activity of the 283

233 participants with impingement syndrome and controls serratus anterior was positively correlated with poste- 284

234 during the push-up-plus exercise. Additionally, Tucker rior tilting of the scapula in participants with mild and 285

235 et al. [19] recently found there were no major differ- severe impingement syndrome. We postulate that the 286

236 ences for the serratus anterior and upper trapezius be- winging or tipping of the scapula is influenced by intra- 287

237 tween athletes with secondary impingement syndrome muscular imbalance of the serratus anterior rather than 288

238 and asymptomatic athletes during closed kinetic exer- just weakness of the serratus anterior, especially in the 289

239 cises. Although it might be difficult to compare the pre- pain-free population. 290

240 vious results with our result directly because impinge- Both the %MVIC and %isolation values of the upper 291

241 ment syndrome has various causes including scapu- trapezius did not differ during the diagonal shoulder- 292

242 lar dyskinesis, both scapular dyskinesis and shoulder elevation and push-up-plus tasks. This differed from 293

243 impingement provoke symptoms during open kinetic previous work, in which altered activation of the up- 294

244 movement such as arm elevation, as this presents a per trapezius characterized participants with abnormal 295

245 different task from closed kinetic movement, such as scapulothoracic movements [24,25]. Participants who 296

246 push-up and push-up-plus tasks, which provides more showed excessive elevation of scapula as dyskinesis 297

247 stability. were excluded from our study due to difficulty of defin- 298

248 We only observed a significant difference in the ing exact mean of excessive elevation, however, the ex- 299

249 %MVIC of the middle serratus anterior during diago- pected compensatory activation of the upper trapezius 300

250 nal shoulder elevation. Participants with scapular dysk- did not occur in participants with winged and tipped 301

251 inesis had significantly increased activation of the mid- scapulae. 302

252 dle serratus anterior compared with the control group, Our study had some limitations. First, although the 303

253 which differs from our hypothesis and another previ- activity of various scapular muscles is correlated with 304

254 ous review study that investigated muscular activation scapulothoracic motion, we only focused on the mid- 305

255 in an impingement group [20]. We thought that in- dle and lower portions of the serratus anterior and up- 306

256 creased activation of middle serratus anterior might in- per trapezius. Second, we could not obtain kinematic 307

257 duced more scapular internal rotation during diagonal data throughout the experiment, so that the accuracy 308

258 elevation, instead of stabilizing the inferior angle of the of diagonal shoulder elevation relied on manual guid- 309

259 scapulae which is provided by the lower parts of ser- ance. Thus, we had no information on the correlation 310

260 ratus anterior. Inman et al. [21] examined integrated between glenohumeral and scapular kinematics among 311

261 EMG data from the scapulothoracic muscles and re- participants with winged and tipped scapula. Finally, 312

262 ported that the trapezius and lower serratus anterior we did not discriminate between scapular winging and 313

263 were the prime movers for normal scapular upward ro- tipping, which have been distinguished as types I and 314

264 tation. Although the difference was not significant, the II scapular dyskinesis in previous studies [26,27]. One 315

265 %MVIC of the lower serratus anterior was lower in the reason of this is that the scapular winging tends to be 316

266 symptomatic group compared with the controls. There- accompanied by scapular tipping. and the reliability of 317

267 fore, we postulated that there is intramuscular imbal- identifying scapular dyskinesis is better with a yes/no 318

268 ance in the serratus anterior in participants with scapu- method than specifically discriminating the types [27]. 319

269 lar winging and tipping, as clearly shown in the %iso-

270 lation data.
271 There was significantly greater %isolation of the 5. Conclusions 320

272 middle serratus anterior and also significantly de-

273 creased values for the lower serratus anterior during di- Our findings indicated that participants with winged 321

274 agonal shoulder elevation. According to the clinical lit- and tipped scapular dyskinesis showed different acti- 322

275 erature, the increased obliquity of a muslce’s pull could vation of the middle and lower serratus anterior com- 323

276 induce a greater portion of the force of the muscle’s pared with controls during the diagonal shoulder ele- 324

277 contraction for stabilizing the joint, rather than mov- vation. These differences may be due to increased ac- 325

278 ing the bone [22]. Our result of the scapular dyskinesis tivation of the middle serratus anterior and decreased 326

279 group showed relatively lower activation of the lower activation of the lower serratus anterior during an open 327

280 serratus anterior and greater activation of the middle kinetic chain activity, which implies that muscular im- 328
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6 S.-Y. Park and W.-G. Yoo / Effect of scapular dykinesis on exercises

329 balance in serratus anterior contributes to winged and slide exercise and other traditional exercises. J Orthop Sports 381

330 tipped scapular dyskinesis. Clinicians might want to Phys Ther. 2006; 36(12): 903-10. 382
[11] Lehman GJ, Gilas D, Patel U. An unstable support surface 383
331 use closed chain exercises in patients with a winged or does not increase scapulothoracic stabilizing muscle ctivity 384
332 tipped scapular for activating the serratus anterior, but during push up and push up plus exercises. Man Ther. 2008; 385
333 this might not be effective for correcting intramuscular 13(6): 500-6. 386

334 imbalance of the serratus anterior during open chain [12] de Oliveira AS, de Morais Carvalho M, de Brum DP. Acti- 387
vation of the shoulder and arm muscles during axial load ex- 388
335 movement. Our results suggest the need to investigate ercises on a stable base of support and on a medicine ball. J 389
336 the parts of the serratus anterior and selective activation Electromyogr Kinesiol. 2008; 18(3): 472-9. 390

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342 Acknowledgments cle: a novel approach for rehabilitation of scapular muscle im- 400
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344 search Program through the National Research Foun- for the serratus anterior and trapezius muscles during surface 404
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