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1 Scapular Muscle Performance in Individuals with Lateral Epicondylalgia

3 Joseph M. Day, PT, PhD, OCS, CIMT


4 Department of Physical Therapy, University of South Alabama, Mobile, AL
5
6 Heather Bush, PhD
7 Department of Biostatistics, University of Kentucky, Lexington, KY
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8
9 Arthur J. Nitz, PT, PhD, ECS, OCS
10 Division of Physical Therapy, University of Kentucky, Lexington, KY
11
12 Tim L. Uhl, ATC, PT, PhD, FNATA
13 Division of Athletic Training, University of Kentucky, Lexington, KY
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14
15 The study protocol was approved by the University of Kentuckys Institutional Review Board.

16

17 The authors certify that they have no affiliations with or financial involvement in any

18 organization or entity with a direct financial interest in the subject matter or materials discussed
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19 in the article.

20
21 Corresponding Author: Joseph M. Day, PhD, MSPT, OCS, CIMT
22 Assistant Professor
23 University of South Alabama
24 Pat Capps Covey College of Allied Health Professions
25 Department of Physical Therapy
26 HAHN 2011
27 5721 USA Drive N.
28 Mobile, AL 36688-0002
29 Phone: (251) 445-9330
30 Fax: (251) 445-9238
31 josephday@southalabama.edu
32
33
34 Study Design: Descriptive, laboratory based, cross sectional study.

35 Objectives: To describe scapular musculature strength, endurance, and change in thickness in

36 individuals with unilateral lateral epicondylalgia (LE) compared to their uninvolved limb and the

37 corresponding limb of a matched comparison group.

38 Background: Reported poor long term outcomes for the non-surgical management of
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39 individuals with LE suggests a less than optimal rehabilitation process. Knowledge of scapular

40 muscle function in a working population of individuals with LE may help further refine

41 conservative management of this condition.

42 Methods: Twenty eight patients with symptomatic LE and 28 controls matched by age and gender were

43 recruited to participate in the study. Strength of the middle trapezius (MT), lower trapezius (LT), and
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44 serratus anterior (SA) was measured with a hand held dynamometer. A scapular isometric muscle

45 endurance task was performed in prone. Changes in muscle thickness of the SA and LT were measured

46 with ultrasound imaging (USI). ANOVA models were used to determine within and between group

47 differences.

48 Results: The involved side of the group with LE had significantly lower values for MT strength
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49 (P=.031), SA strength (P<.001), LT strength (P= .006), endurance (P = .003), and change in SA

50 thickness (P = .028) when compared to the corresponding limb of the control group. The

51 involved side of the group with LE had significantly lower strength of the LT (P = .023) and SA

52 (P = .016) when compared to their uninvolved limb, however these differences were small and of

53 potentially limited clinical significance.

54 Conclusion: When compared to a matched comparison group, there were impairments of

55 scapular musculature strength and endurance in patients with LE, suggesting that the scapular

56 musculature should be assessed and potentially treated in this population. Cause and effect

57 cannot be established as the weakness of the scapular musculature could be a result of LE.
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60
59
58
Key Words: serratus anterior, strength, trapezius, ultrasound imaging
61 Lateral epicondylalgia (LE), originally described as lawn tennis elbow,36 is characterized

62 by pain in the region of the lateral epicondyle of the humerus.29 While a high percentage of

63 recreational tennis players develop the pathology,20 LE is also a common condition with

64 significant negative consequence in the general population. The prevalence of LE has been

65 reported to be as high as 12.2% in occupational settings.46 In addition, 27% of patients with LE


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66 report severe limitations with activities of daily living,52 such as lifting bags or boxes.53

67 The effectiveness of conservative treatment approaches remains less than optimal

68 secondary to high recurrence rates. Cortisone injections are effective in pain management but

69 only up to 8 weeks from the time of the injection.11, 22, 40, 41 A recent study reported between a

70 29% to 38% recurrence rate in individuals receiving conservative treatment.10 In the only study
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71 with a 2 year follow after physiotherapy intervention, more than half the patients reported

72 ongoing pain and functional lost, secondary to return of LE symptoms.38

73 It has been suggested that assessing scapular muscle impairments should be an important

74 component of in the evaluation of individuals with LE. Lucado et al30 recently reported
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75 diminished lower trapezius (LT) muscle strength in a group of female tennis players with LE

76 compared to a matched group of asymptomatic female tennis players.30 In a healthy population

77 of throwing athletes, fatigue of the scapular stabilizers has been shown to produce alterations of

78 elbow kinematics,25, 29 implying that scapular muscle fatigue could predispose individuals to

79 throwing injuries at the elbow region. Another investigator reported that induced pain at the

80 upper trapezius (UT) produces an increase in wrist extensor electromyographic (EMG) signal

81 intensity in healthy individuals,45 which could potentially lead to an overuse injury, such as LE,

82 at the elbow. Anecdotally, our clinical experience suggest that overuse of the UT and underuse

83 of the LT, may result in UT pain.


84 Although it appears that scapular musculature strength and endurance has a potential

85 influence on patients with LE, data are limited to a population of female tennis players30 and a

86 case report.5 Because there is a high prevalence of LE in the working population,46 and most

87 studies report that males will develop the condition just as frequently as females,21 there is a need

88 to investigate scapular muscle strength in a more inclusive group of patients. In addition,


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89 although the study by Hidetomo et al,25 implies that fatigued scapular muscles may contribute to

90 elbow pathology, no studies have directly investigated scapular muscle endurance on patients

91 with LE.

92 The primary purpose of this study was to compare scapular musculature strength,

93 endurance, and change in thickness from resting to contraction, as measured by RUSI, of patients
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94 with unilateral LE with the corresponding limb of a matched comparison group. The secondary

95 purpose was to compare the same variables between the involved and uninvolved limb of the

96 group with unilateral LE.

97
98 METHODS
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99 Participants

100 A sample of convenience of 28 patients with unilateral LE (15 females, 13 males) and 28

101 age and gender matched controls agreed to participate in the study (FIGURE 1). Patients were

102 recruited from 1 of 5 outpatient rehabilitation clinics in central Kentucky and controls were

103 recruited from the central Kentucky region.

104 Patients were recruited to participate in this study if they: were seeking medical attention

105 from a therapist at 1 of 5 outpatient clinics, reported a primary symptom of unilateral lateral

106 elbow pain, were between the ages of 18 and 65, and if they presented with at least 2 positive

107 clinical tests for LE. The clinical tests performed for symptoms of LE were: palpation of the
108 lateral epicondyle and the associated common wrist extensor unit, passive stretching of the wrist

109 extensors (Mills sign), strength assessment with a hand grip dynamometer, manual resistance

110 against maximal volitional contraction (MVIC) of the wrist extensors (Cozens sign), and

111 manual resistance applied to extension of the middle digit (Maudsleys test).8, 18 The clinical tests

112 were considered positive if there was reproduction of pain at the lateral epicondyle.
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113 Patients were excluded from the study if they reported any of the following as part of

114 their medical history: peripheral neuropathy secondary to diabetes, progressive neurological

115 disorder, cancer, infection in spine or upper extremity, upper motor neurological disorder (eg,

116 stroke, traumatic brain injury), or fibromyalgia. Patients were also excluded if they had surgery

117 on the upper quadrant within the previous 6 months or if they had a score of less than 10% on the
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118 quick version of the disabilities of the arm, shoulder, and hand questionnaire (QuickDASH). This

119 last exclusion was based on a previous study indicating that DASH scores typically range from 0

120 to 10.1% in the general population.26

121 For those in the comparison group, the tests for LE were performed and the disability
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122 score was also recorded during the initial intake. Potentials participants for the control group

123 were excluded from the study if they reported: any current or history of upper quadrant

124 musculoskeletal conditions within the past 6 months, had trunk or upper quadrant surgery in the

125 previous 6 months, tested positive for any of the tests for LE, or had a disability score of greater

126 than 10% as measured by the QuickDASH.26

127 To be included in the study, all potential participants had to demonstrate the ability to

128 tolerate and maintain the instructed test positions. All participants gave their written, informed

129 consent to take part in the study and the study protocol was approved by the University of

130 Kentuckys Institutional Review Board. Participants rights were protected.


131 Procedures

132 All measures of scapular muscle strength were performed by the primary investigator

133 who was not blinded to the participants group assignment or to the knowledge of the involved

134 limb for the patients with LE. Before the first dependent variable was measured, a baseline

135 resting heart rate was obtained. For the purpose of this study, heart rate was assessed to examine
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136 the arousal factors related to the muscle performance tests. A 5 minute rest period was given to

137 the participant after each group of dependent variables was measured to allow time for

138 recovery.42, 48 Heart rate was measured immediately after data collection of each group of

139 dependent variables and then after the allotted 5 minute rest to ensure the participant had

140 recovered to baseline values. Extra rest was given if the participant did not return to baseline
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141 values.

142 Microsoft Excel 2007 was used to generate a random list of numbers to determine the

143 order for scapular muscle testing (thickness measures with USI, hand held dynamometer (HHD)

144 testing, and endurance testing). The order of each outcome measure within each scapular test and
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145 the first limb tested (dominant versus non-dominant) was also determined from a random list of

146 numbers.

147 Strength Testing Prior to the study, a Nicholas manual muscle HHD (model 01160, Lafayette

148 Instrument Co.) was calibrated by placing weights of 15lbs (6.8kg), 25lbs (11.3kg), and 50lbs

149 (22.7kg) on the dynamometer and then calculating the absolute difference between the expected

150 value of the weight and observed value on the dynamometer. The largest difference between

151 measures was .14kgs.

152 Previously established methods for measuring strength of scapular muscles using a HHD

153 report good between day intrarater reliability (ICC = .75 to .97),7, 33 however, no validity data
154 have been established for measuring MT or SA strength. MVICs for both the left and right upper

155 extremities were assessed. Each patient performed a practice trial on the affected upper extremity

156 for each test before data were recorded. The investigator instructed the participant to slowly push

157 into the dynamometer and increase force production to the maximum force by the end of the 5

158 seconds used for testing. The MVIC was recorded by the assessor. The following muscles were
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159 tested: MT, LT, and SA.33 Three trials were performed for each muscle and the average value of

160 the 3 trials was used for statistical analysis.

161 The SA was tested by positioning the participant supine with the shoulder and elbow

162 flexed to 90. The dynamometer was placed on the olecranon of the elbow. The patient was

163 asked to protract the scapula and resistance was given along the humeral axis (FIGURE 2). For
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164 the MT, the participant was positioned prone with the elbow flexed and shoulder held to 90

165 abduction. The dynamometer was placed on the spine of the scapula, in between the acromion

166 and the medial superior border of the scapula. The participant was instructed to lift the arm

167 upward, while resistance with the dynamometer was being applied in the lateral direction
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168 (FIGURE 2). Finally, the LT was tested by positioning the participant prone with arm extended

169 and shoulder held to 135 of abduction. The dynamometer was placed in the middle of the

170 scapula, in between the acromion and the medial superior border. While the participant lifted

171 his/her arm upward, resistance with the dynamometer was applied in the lateral and superior

172 direction (FIGURE 2). For both the MT and LT, the investigator was positioned on the opposite

173 side of the limb to be tested.16, 33

174 Scapular Muscle Endurance Lying prone, the participant was asked to place their forehead on

175 the contralateral limb. The limb to be tested was passively positioned to 135 of shoulder

176 abduction. The test position was chosen because EMG analysis demonstrates that the LT, MT,
177 UT, and SA, are active in this position.9, 15, 37 A cuff weight of 1% of the participants body

178 weight (to the nearest 0.23 kg) was strapped just proximal to the elbow. A level was positioned

179 at a height parallel to the trunk and at 135 of shoulder horizontal abduction. The participant was

180 then asked to elevate and hold their arm to the established level for as long possible (FIGURE

181 3). The test was terminated when the participant voluntarily lowered their upper extremity or if
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182 the distal radius was no longer contacting the level.27, 49 A single trial was performed and its

183 value used for statistical analysis.

184 Muscle thickness The primary investigator received formal training through The Burwin Institute

185 of Diagnostic Medical Ultrasound. Data were collected on 18 of the 28 available patients and

186 controls. Participants were not preferentially chosen by the researchers but were instead based
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187 on the participants time constraints or equipment availability.

188 Methods for positioning and landmark identification were based on a recently published

189 reliability study.12 Participants were seated comfortably on a chair without a back rest. A neutral

190 spine posture was established by instructing the participant to sit upright and then slump 3 times.
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191 After the third movement, the researcher asked the participant to rest comfortably between the 2

192 motions.31 The participant was then asked to place their forearm on an adjustable table that was

193 adjusted to place the arm at 85 of shoulder elevation and 45shoulder horizontal adduction

194 (FIGURE 4). Horizontal adduction was maintained throughout testing by placing a mark for arm

195 position which was continuously monitored during testing. A felt tip pen was used to mark the

196 level of the thoracic spine that coincided with the inferior angle of the scapula so that the

197 ultrasound transducer could be placed in a consistent position for all measures.39 Additionally a

198 mark was placed on the lateral torso at the level of the inferior angle of the scapula between the

199 pectoralis major and the latissimus dorsi indicating the location of the serratus anterior.4
200 Computerized ultrasonography (General Electric LOGIQ e 2008) was used by the

201 primary investigator to produce a cross sectional image of the LT and SA at rest and during arm

202 lifting (FIGURE 4). In B mode, a 40 mm 8-MHz linear transducer was placed transversely over

203 the mark previously made to identify the LT and vertically along the mark used to identify the

204 SA. A 2.27 kg (5 lbs) weight was strapped around the arm of each participant, just proximal to
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205 the elbow. This load was found to be equivalent to holding a 0.91 kg (2 lbs) weight in the hand.

206 In pilot work performed prior to this investigation, a load of 0.91kg held in the hand was

207 observed to produce a consistent visual increase in muscle thickness of the LT and SA, when

208 compared to their resting state.

209 Initially, an image was taken with the muscle in a resting state. Second, the participant
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210 was asked to elevate their arm with the elbow extended to 0, shoulder horizontally adducted to

211 45 from the frontal plane, shoulder flexed at 90, and shoulder externally rotated (thumb up

212 position). This position is known to produce high SA and moderate LT activity15, 16, 37 and was

213 chosen over shoulder protraction because elevation of the arm in the scapular plane is a more
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214 functional position. The arm was then held for approximately 2 seconds to allow an ultrasound

215 image to be taken. A second resting and lifting image was subsequently taken for the same arm

216 and muscle using the same procedure. The same procedure was then followed to test the same

217 muscle on the contralateral limb. The entire procedure was then repeated for testing of the other

218 muscle for both limbs.

219 Muscle thickness measurements were performed using procedures based on a previous

220 study.12 Two images were taken of each muscle for both the relaxed condition and contracted

221 condition.28 Linear measurements of LT thickness were made 2 cm from the spinous process

222 landmark.39 Linear measurements of SA thickness were made from the inside border of the rib
223 up to the inside edge of the muscle border. The rib served as the on-screen anatomical reference.

224 The average of 5 thickness measures, spanning the width of the rib, was recorded.12 Prior to

225 statistical analysis, the measures obtained from the 2 images of the same person, condition, and

226 muscle were averaged together for one data point.

227 Two patients were excluded from the SA USI analysis secondary to poor image quality
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228 taken during data collection. Therefore, a total of 18 (11 female, 7 males) patients were included

229 for the LT USI data analysis and 16 (10 female, 6 male) for the SA USI data analysis. Eighteen

230 controls were matched by age and gender to the patient population. The average of 2 measures

231 of LT absolute thickness was the dependent measure in one model and the SA absolute thickness

232 was the other dependent measure examined.


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233 Statistical Analyses

234 An a priori power analysis was completed based on previous measures of scapular

235 muscle strength which indicated that a minimal detectable change (MDC) of 3.6 kg can identify

236 true difference between tests for the SA. An effect size of .60 was calculated by dividing the
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237 MDC value of 3.6 kg by the reported standard deviation of 6.0 kg for the SA. The SA effect size

238 of .60 was chosen for the power analysis because this value was smaller than the effect sizes of

239 the LT and MT.33 Using an effect size of .60, a sample size of 28 participants in each group

240 provided a true power of 86% conducted at alpha = .05.

241 Statistical Analysis was performed using SPSS version 20 for windows (SPSS Inc.

242 Chicago, IL). Descriptive data for mechanism of injury and duration of symptoms was

243 calculated for patients with LE. In addition, descriptive data were calculated for the QuickDASH

244 and all dependent variables for both groups. To evaluate similarity between the control and
245 patient groups, paired t tests were used to compare age, body mass, height, and shoulder activity

246 levels.

247 Between group comparisons for Strength and Endurance variables For this comparison, the

248 involved limb of the patient group was compared to the matched limb, based on arm dominance

249 of the patient, of the control group. For each dependent measure (MT strength, LT strength, SA
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250 strength, and endurance) separate linear mixed models were run using 1 within-group factor,

251 group (patient or control), and 1 between-group factor, dominance (whether the involved limb

252 from the patient group and matched limb from the control group was dominant or non-

253 dominant). Dominance of the analyzed limb had to be considered for both groups as statistical

254 difference due to limb dominance has previously been established for healthy individuals.
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255 Finally, because our control participants were not matched according to height and weight, these

256 2 variables were used as covariates in each model. A P-value of .05 was set a priori. In the case

257 of an interaction, a least significant difference (LSD) post hoc analysis was performed. If no

258 significant interaction was present, the model was run again without the interaction so that the
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259 other factors could be interpreted.

260

261 Between group comparisons for Muscle Thickness variables Similar to the above strength and

262 endurance analysis, only one limb was analyzed per group (the involved limb of the patient

263 group and the matched limb, based on arm dominance of the patient, of the control group). The

264 other element of the primary purpose was to investigate the differences in muscle thickness

265 (contracting thickness minus resting thickness) of the LT and SA between patients with LE and

266 controls. Separate linear mixed models were used using 2 within-group factors (1) condition (rest

267 and contraction) and (2) group (patient and control). Dominance (whether the involved limb
268 from the patient group and matched limb from the control group was dominant or non-dominant)

269 was used as a between-group factor. Height and weight were also used as covariates in each

270 model. A P-value of .05 was set a priori. In the case of an interaction, a LSD post hoc analysis

271 was performed. If no significant interaction was present, the model was run again without the

272 interaction so that the rest of the factors could be interpreted.


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273

274 Within group comparisons (LE group) for Strength and Endurance variables For each

275 dependent measure (MT strength, LT strength, SA strength, and endurance) separate linear

276 mixed models were run using 1 within-group factor, limb (uninvolved or involved), and 1

277 between-group factor, dominance (dominant involved or non-dominant involved). A P-value of


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278 .05 was set a priori. In the case of an interaction, a LSD post hoc analysis was performed. If no

279 significant interaction was present, the model was run again without the interaction so that the

280 other factors could be interpreted.

281
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282 Within group comparisons (LE group) for muscle thickness variables The other element of the

283 secondary purpose was to investigate the differences in muscle thickness of the LT and SA

284 between involved and uninvolved limbs. Separate linear mixed models were used using 2 within-

285 group factors (1) condition (rest and contraction), and (2) limb (uninvolved and involved).

286 Dominance (dominant involved or non-dominant involved) was used as a between-group factor.

287 A P-value of .05 was set a priori. In the case of an interaction, a - LSD post hoc analysis was

288 performed. If no significant interaction was present, the model was run again without the

289 interaction so that the other factors could be interpreted.

290
291 RESULTS

292 Age, height, and shoulder activity levels were not statistically different between groups.

293 Those with LE were found to have higher QuickDASH scores (P<.001) than those in the control

294 group (TABLES 1 and 2). Among patients with LE, 79% reported an insidious onset, whereas

295 21% reported a specific event that caused the injury. In patients with LE the median
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296 (interquartile range) duration of symptoms was 12 (8 to 22) weeks and 15 of 28 (53%)

297 participants reported the affected side as their dominant side. The descriptive (unadjusted) data

298 for strength, endurance, and USI measures are provided in TABLES 3, 4, and 5.

299

300 Comparisons between groups


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301 Strength There was no significant interactions between group and dominance when accounting

302 for the participants height and weight (P>.503). There were no differences in limb dominance

303 regardless of group (P>.535). However, the control group was stronger than the LE group for the

304 LT (P=.006), MT (P=.031), and SA (P <.001; FIGURE 5).


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305 Endurance Similar to strength, there was no significant interactions between group and

306 dominance when accounting for participants height and weight (P = .775) and there were no

307 differences in limb dominance regardless of group (P = .740). The control group had greater

308 endurance than the LE group (P=.003; FIGURE 6)

309 Muscle Thickness For SA, there was no significant 3 way interaction between muscle type,

310 group, and dominance (P = .11). There was a significant 2 way interaction (P=.028) between SA

311 thickness condition and group when accounting for the participants height and weight. The

312 marginal means indicate that those in the control group had a greater change in SA thickness (1.4

313 mm) relative to patients with LE (0.7 mm; TABLE 6). Post hoc analysis revealed a significant
314 increase in thickness from rest to a contracted condition for the LE (P<.001) and control

315 (P=.015) groups. No significant differences were found between patients with LE and control

316 group for resting SA thickness (P = .919) or contracting thicknesses (P= .248). The statistical

317 analysis for the LT muscle indicates no 3 way (P=.155) or 2 way interaction for group and type

318 (P = .580). There was a significant increase in thickness from rest to a contracted condition
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319 regardless of groups (P<.001, TABLE 6).

320

321 LE Involved to Uninvolved Comparison

322 Strength There were no significant interactions between limb and dominance (P >.381). There

323 were no differences in dominance regardless of group (P>.524). In addition, there was no
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324 significant difference in involved versus uninvolved muscle strength for the MT (P=.26).

325 However, the involved limb was weaker than the uninvolved limb when measuring SA strength

326 (P =.016) and LT strength (P = .023, FIGURE 7)

327 Endurance Similar to our within group results for strength, there was no interaction between
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328 limb and dominance (P = .178) and no differences in dominance regardless of whether the limb

329 was involved or uninvolved (P = .587). There were no differences in endurance times when

330 comparing the uninvolved and involved limbs (Noninvolved = 64 +/- 34 s, Involved = 53 +/- 41

331 s; P=.096).

332 Muscle Thickness For both the SA and LT, there were no significant 3 way interactions between

333 muscle type, limb, and dominance (P >.071) or 2 way interactions between type and limb (P

334 >.444). There was a significant increase in thickness from rest to a contracted condition

335 regardless of group (P<.001) for both muscles (TABLE 7).


336

337 DISCUSSION

338 To our knowledge, this is the first study to investigate scapular muscle characteristics in a

339 general population of patients with LE. Consistent with our primary hypothesis, SA strength, LT

340 strength, MT strength, scapular muscle endurance, and change in SA muscle thickness in patients
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341 with LE were significantly less than for the matched comparison group. The findings suggest

342 that therapists should consider factors that impact scapular muscle performance (strength and

343 endurance) in patients with LE.

344 While our results indicated that scapular muscle strength and endurance was impaired in

345 patients with LE compared to matched controls, when comparing the patients involved limb to
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346 their uninvolved limb, the differences, although statistically significant and only for SA and LT

347 strength, do not exceed measurement error using a HHD. These 2 findings are consistent with

348 previous cross sectional studies on patients with LE.1, 30 Most closely related to our study,

349 Lucado et al30 found significantly lower LT strength in female tennis players with LE compared
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350 to healthy female tennis players. In a second study, Alizadehkhaiyat et al1 assessed isometric

351 strength for select shoulder muscles in patients with LE comparing the results to matched

352 controls and also to the patients uninvolved side. Similar to our study, the authors found that

353 there were deficits in strength when comparing patients with LE to matched controls but no

354 meaningful differences in shoulder strength between the uninvolved and involved limbs.1

355 The current study also demonstrates diminished scapular muscle endurance in patients

356 with LE. There has been very little literature published with which to compare our endurance

357 results. Alizadehkhaiyat et al3 found no significant differences in rotator cuff muscle endurance

358 compared to a control group. The differences in findings between studies may be attributed to the
359 type of endurance task performed. Alizadehkhaiyat et al1 investigated repetitive isotonic

360 shoulder contractions compared to the current study in which sustained isometric contraction was

361 used to measure fatigue. The 2 types of endurance tests physiologically differ. Intramuscular

362 tissue pressure (MTP) increases during sustained isometric contractions and MTP is known to

363 interfere with muscular blood flow.14, 44 The impeded blood flow could result in muscle ischemia
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364 thus altering muscle performance.32, 47 Diminished oxygen delivery will accelerate muscle

365 fatigue compared to the isotonic test where the muscle acts as a natural pump for blood flow.

366 Thus, the differences observed in isometric endurance times in the current study, may be a

367 difference in muscle perfusion efficiency between patients with LE and controls.

368 The position of this endurance test, prone shoulder abduction at 135, was chosen by the
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369 investigators because it is known to produce a high amount of LT activity.15, 16, 37 However, it

370 could be argued that because other posterior shoulder muscles are also active in this position, the

371 described test may not be a true measure of LT endurance. Therefore, future research is needed

372 to better determine which of the posterior shoulder muscles are most affected by this test
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373 position. Previous studies have compared rate of median frequency shifts between muscles to

374 show which muscle is fatigued at a greater rate. 35 Although factors like muscle strength and the

375 contribution of synergistic muscles would have to be considered, comparing rates of median

376 frequency shifts could be used to determine which of the several posterior shoulder muscles are

377 fatiguing the fastest.

378 Our findings have implications to clinical practice. The differences in LT strength (25 N)

379 and SA strength (72 N) between patients with LE and controls meet or exceed the MDC values

380 from previously published data.33 The mean values indicate that the differences are beyond

381 measurement error of the device used. Although MDC values for the described scapular muscle
382 endurance test have never been published, the mean difference between patients with LE and

383 controls are large (31 seconds) and statistically significant. As a result, addressing LT strength,

384 SA strength, as well as scapular muscle endurance should be considered in patients with LE.

385 In contrast to the above finding, there were no measureable differences between patients

386 involved and uninvolved limbs. Because a limb to limb comparison in the clinical setting is often
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387 the most convenient approach to assess patients, scapular muscle impairments may be missed.

388 Therefore, to determine the presence of deficits, clinicians should compare strength and

389 endurance findings in patients with LE to normative data, yet to be established.

390 The assessment of scapular muscle strength and endurance is potentially important in

391 patients with LE to provide clinicians with objective information to make a clinical decision as to
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392 whether treatment is indicated. Based on this study design, we are unable to definitively

393 determine if treating scapular muscle strength and endurance deficits will improve outcomes in

394 patients with LE. However, Bhatt et al5 reported successful treatment of a 54 year old female

395 with only strengthening exercises targeting the middle and lower trapezius muscles. It has also
Journal of Orthopaedic & Sports Physical Therapy

396 been reported that after successful remission of pain symptoms, patients previously diagnosed

397 with LE continue to present with shoulder weakness.2 During functional arm motions, kinetic

398 energy is transferred from proximal to more distal segments of the arm. With an impaired ability

399 to stabilize the scapula, increased energy demands are theoretically required of tissues in the

400 distal upper extremity when performing a functional activity.17, 43 Theoretically, the

401 scapulothoracic muscle impairments found in this study could perpetuate the LE or predispose

402 patients to re-injury if left unaddressed.

403 Notwithstanding, the design of this study does not allow for definitive conclusions that

404 scapular muscle weakness is a causative factor for the development of LE. One other possible
405 theory is that lateral epicondyle pain triggers a centrally mediated mechanism resulting in the

406 observed scapular muscle weakness. To that end, muscle inhibition from a regional source of

407 pain has been reported for the quadriceps,19, 51 hamstrings,24 and masseter34 muscles. In addition,

408 pain of the common wrist extensors may cause the patient to use the upper extremity less and in

409 a more guarded range of motion. Over time, disuse would result in decrease in shoulder active
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410 range of motion and weakness of the shoulder musculature.

411 Future studies are needed to more completely define the clinical significance of scapular

412 muscle deficits in patients with LE. Because it could be argued that the differences in muscle

413 strength could be a difference solely of scapular and thoracic posture. Future studies should

414 assess the spinal curvature and position of the scapula in both populations and then see if the
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415 testing position equally impacts both groups. In addition, it would be interesting to determine if

416 treating scapular muscle deficits will improve both short and long term outcomes in patients with

417 LE. Prospective studies are also warranted to determine if scapular muscle weakness is present

418 prior to the development of LE and if scapular muscle weakness is a potential risk factor for LE.
Journal of Orthopaedic & Sports Physical Therapy

419 The results of our study highlight that the change in SA thickness from rest to contraction

420 was significantly different between patients with LE and controls, but no differences were found

421 comparing the involved SA with the uninvolved SA. In addition, using this methodology, the

422 change in LT does not appear to behave differently in patients with LE compared to normal

423 controls or when comparing a patients involved LT with the uninvolved LT. Preliminarily, the

424 differences observed between patients with LE and controls for the change scores from rest to

425 contraction is encouraging and warrants further investigation, but there is a number of limitations

426 to the interpretation of USI of muscle actions. 55


427 In the EMG literature, it has been consistently reported that individuals with cervical

428 pain, shoulder pain, and postural deficits demonstrate diminished SA activity compared to

429 controls, while results for LT activity have been inconsistent.13, 23, 50, 54 Overall, the findings in

430 our study and in previous studies may indicate that individuals with upper quarter pain or

431 postural deficits often present with diminished SA function. Future research should examine
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432 whether the observed SA deficits are a result of a specific pathology or are a predetermining

433 factor in the development of conditions like cervical, shoulder, and lateral elbow pain.

434 Limitations

435 Despite efforts made to eliminate extraneous factors influencing the results of our study,

436 there are several limitations that should be considered. First, all measures of scapular muscle
Copyright ${year} Journal of Orthopaedic & Sports Physical Therapy. All rights reserved.

437 strength were performed by the primary investigator and the investigator was not blinded to

438 neither group assignment nor the involved limb in patients with LE, thus introducing potential

439 investigator bias. In addition, it has been demonstrated by EMG analysis that the SA strength test

440 used in this study does not isolate SA function, and therefore the test may be better regarded as a
Journal of Orthopaedic & Sports Physical Therapy

441 indicating scapulothoracic protraction weakness.33 Second, a submaximal endurance task as

442 completed in this study is thought to be influenced by an individuals ability to self-regulate.

443 Self-regulation can cause an individual to override a feeling of fatigue, through the central

444 nervous system, to sustain an endurance task.6 Therefore, it is possible that individuals with LE

445 have a diminished ability to self-regulate, thus reducing the endurance times. Third, because the

446 patients have pain and no systematic differences were detected between limbs, it is possible that

447 pain is a central drive factor for MVIC, endurance, and muscle thickness measures. Fourth, the

448 power analysis suggested that 28 participants be recruited for this study but only 18 were

449 available for the USI assessment. Finally, it is difficult to ascertain the exact meaning of change
450 in muscle thickness using USI because of the inconsistent findings reported by previous authors

451 looking at the correlations between change in muscle thickness and muscle activity.55

452

453 CONCLUSION

454 Patients with LE demonstrated significant weakness of the LT and SA as well as a


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455 significant decline in scapular muscle endurance when compared to an asymptomatic control

456 group. Assessment of SA strength, LT strength, and posterior shoulder muscle endurance is

457 recommended in patients with LE. Future studies should seek to investigate the short and long

458 term efficacy of treating scapular muscle deficits as part of a comprehensive treatment program

459 for individuals with LE.


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460
461 KEY POINTS
462
463 Findings: Patients with LE demonstrated significant weakness of the LT and SA as well as a

464 significant decline in scapular muscle endurance when compared to an asymptomatic control

465 group. The differences between a patients uninvolved and involved limb were not clinically
Journal of Orthopaedic & Sports Physical Therapy

466 meaningful.

467 Implications: Scapular muscle strength and endurance deficits should be considered in the

468 management of patients with lateral elbow pain.

469 Caution: This was a cross-sectional study of a small group of patients with LE; therefore, the

470 data do not indicate a causal relationship between LE and scapular muscle weakness.

471

472 Acknowledgements: We thank the therapist and staff at Kentucky Hand and Physical Therapy

473 for their participation in patient recruitment and Dr. Joe Stemple for his editorial comments on

474 the manuscript.


475 References

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585 Term, but Harmful in the Longer Term; Data for Non-Corticosteroid Injections and Other
586 Tendinopathies Are Limited. Evid Based Med. 2011;16:116-117.
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594 Acute Experimental Pain in Trapezius and Sored Wrist Extensor on the
595 Electromyography of the Forearm Muscles During Computer Work. Appl Ergon.
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614 Epicondylitis: A Population-Based Study. Rheumatology (Oxford). 2012;51:305-310.
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620 Ther. 2010;14:367-374.


621 55. Whittaker JL, Stokes M. Ultrasound Imaging and Muscle Function. J Orthop Sports Phys
622 Ther. 2011;41:572-580.
623

624

625
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626

Variables Patients with LE Controls


(n=28) (n=28)
Age, y 46.8 +/- 8.8 46.1 +/- 9.2

Body mass, kg* 83.8 +/- 15.9 73.3 +/- 13.3

Height, m 1.70 +/- 0.10 1.71 +/- 0.09


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Shoulder Activity Level (0-20) 10.3 +/- 4.1 10.8 +/- 4.2

QuickDASH, %* 40.6 +/- 16.3 2.6 +/- 3.5

627 TABLE 1: Characteristics of participants with Strength and Endurance data.


628 Abbreviations: LE, lateral epicondylalgia; QuickDASH, quick version of the disability of the arm, shoulder, and
629 hand questionnaire. Values are means +/- standard deviations. Shoulder Activity Level is based on a scale from 0
630 (no shoulder activity) to 20 (highest shoulder activity). * Indicates a significant difference between groups (P<.05)
631
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632

633

Variables Patients with LE Controls


(n=18) (n=18)
Age, y 48.2 +/- 9.8 48.0 +/- 10.2

Body mass, kg* 83.9 +/- 17.3 69.9 +/- 13.0


Journal of Orthopaedic & Sports Physical Therapy

Height, m 1.67 +/- 0.11 1.71 +/- 0.08

Shoulder Activity Level (0-10) 10.5 +/- 3.9 11.5 +/- 4.0

QuickDASH, %* 38.4 +/- 16.8 2.0 +/- 3.1

634 TABLE 2: Characteristics of participants with Muscle Thickness data.


635 Abbreviation: LE, lateral epicondylalgia; QuickDASH, quick version of the disability of the arm, shoulder, and hand
636 questionnaire. Values are means +/- standard deviations. Shoulder Activity Level is based on a scale from 0 (no
637 shoulder activity) to 20 (highest shoulder activity). *Indicates a significant difference between groups (P<.05)
638

639
640

641
Measure Patients with LE (n=28) Controls (n=28)

Uninvolved Involved Matched limb

LT Strength (N) 123 +/- 25 109 +/- 37 125 +/- 29

MT Strength (N) 146 +/- 27 139 +/- 38 149 +/- 25

SA Strength (N) 205 +/- 51 185 +/- 66 244 +/- 49


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Endurance (s) 64 +/- 41 54 +/- 34 85 +/- 34

642 TABLE 3: Scapular muscle strength and endurance. Data are unadjusted means +/- standard deviations.
643 Unadjusted means are raw data and do not consider arm dominance, weight, and height.
644 Abbreviations: LE, lateral epicondylalgia; LT, lower trapezius; MT, middle trapezius; SA, serratus anterior. Values
645 displayed for the control group represents a matched limb to a patient with LE. Matching was based on arm
646 dominance.
647
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648

Muscle
Patients with LE Control
Relaxed Contracted Difference Relaxed Contracted Difference
Serratus Anterior 5.9 +/-2.4 6.6 +/- 2.3 0.7 4.9 +/- 1.6 6.3 +/- 1.6 1.4
Lower Trapezius 5.1 +/- 2.0 6.5 +/- 2.1 1.4 4.3 +/- 2.0 5.6 +/- 2.0 1.3
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649 TABLE 4: Scapular Muscle Thickness. Data are unadjusted means +/- standard deviations in mm. Unadjusted
650 means are raw data and do not consider arm dominance, weight, and height. Abbreviation: LE, lateral
651 epicondylalgia. Values displayed for the control group represents a matched limb to a patient with LE. Matching
652 was based on arm dominance. N=16 for the serratus anterior, N=18 for the lower trapezius.

653
654

Muscle
Uninvolved Limb Involved Limb
Relaxed Contracted Difference Relaxed Contracted Difference
Serratus Anterior 5.9 +/- 2.3 6.6 +/- 2.5 0.7 5.9 +/- 2.4 6.6 +/- 2.3 0.7
Lower Trapezius 5.3 +/- 2.0 6.4 +/- 2.3 1.1 5.1 +/- 2.0 6.5 +/- 2.1 1.4
655 TABLE 5: Within Group Comparison of Scapular Muscle Thickness for the group with lateral
656 epicondylalgia. Data are unadjusted means +/- SD in mm. Unadjusted means are raw data and do not consider arm
657 dominance. N=16 for the serratus anterior, N=18 for the lower trapezius.

658
659

Muscle
Patients with LE Controls
Relaxed Contracted Difference Relaxed Contracted Difference
Serratus Anterior 5.4 +/1.6 6.1 +/- 2.0 0.7* 5.4 +/- 1.2 6.8 +/ 1.6 1.4*
Lower Trapezius 4.6 +/1.7 6.0 +/- 1.9 1.4* 4.8 +/- 1.4 6.1 +/-1.7 1.3*
660 TABLE 6: Between Group Comparison of Marginal Mean Values of Scapular Muscle Thickness.
661 Data are adjusted means +/- standard deviations values in mm when considering arm dominance, height, and weight.
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662 Values displayed for the control group represents a matched limb to a patient with LE. Matching was based on arm
663 dominance. N=16 for the serratus anterior, N=18 for the lower trapezius.
664 Abbreviation: LE, lateral epicondylalgia.
665 * Indicates a significant increase from rest to contraction.
666 Indicates that there was a significant 2 way interaction (P=.028) between serratus anterior thickness condition and
667 group, showing that the controls had a greater change in thickness with contraction.
668

669
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Muscle
Uninvolved Limb Involved Limb
Relaxed Contracted Difference Relaxed Contracted Difference
SerratusAnterior 5.9 +/- 2.3 6.6 +/- 2.5 1.7* 5.9 +/- 2.5 6.8 +/- 2.9 0.9*
Lower Trapezius 5.1 +/- 2.1 6.5 +/- 2.3 1.4* 5.0 +/- 1.9 6.4 +/- 2.7 1.4*
670 TABLE 7: Within Group Comparison of Marginal Mean Values of Scapular Muscle Thickness for the group
671 with lateral epicondylalgia. Marginal Means +/- standard deviations in mm are the adjusted mean values when
Journal of Orthopaedic & Sports Physical Therapy

672 also considering arm dominance. N=16 for the serratus anterior, N=18 for the lower trapezius. * Indicates a
673 significant increase from rest to contraction (P<.001).

674
675

676
677

678

679

680

681

682
683

684 Patients Controls


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685
Journal of Orthopaedic & Sports Physical Therapy

686 FIGURE 1: Participant recruitment and testing flow diagram. Disability scores were based on the Quick
687 version of the Disability of the Arm, Shoulder and Hand questionnaire. Abbreviations: LT, lower trapezius; SA,
688 serratus anterior; USI, ultrasound imaging

689
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698
697
696
695
694
693
692
691
690

C
B

A = Middle Trapezius, B= Lower Trapezius, C= Serratus Anterior


FIGURE 2: Positioning for strength testing using the hand held dynamometer.
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FIGURE 3: Scapular Muscle Endurance Testing.

placement for ultrasound imaging of the lower trapezius12


FIGURE 4A: Resting position of the participant and probe
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FIGURE 4B: Resting position of the participant and probe


placement for ultrasound imaging of the serratus anterior12
*

*
*
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FIGURE 5: Scapular Muscle Strength. Data are marginal means +/- standard deviations (adjusted for height and
weight). Measures represent the involved limb of the patients with LE and a matched limb of the control group. The
matched limb of the control group was based on arm dominance. Abbreviations: LE, lateral epicondylalgia; LT,
lower trapezius; MT, middle trapezius; SA, serratus anterior. Data: LT Control = 130 +/- 29 N; LT Patient = 104 +/-
33 N; MT Control = 152 +/- 22 N; MT Patient = 135 +/- 33 N; SA Control = 250 +/- 50 N; SA Patient = 178 +/- 62
N. * Indicates a significant difference between groups (P<.01).
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FIGURE 6: Scapular Muscle Endurance. Data are marginal means +/- standard deviations (adjusted for height
Copyright ${year} Journal of Orthopaedic & Sports Physical Therapy. All rights reserved.

and weight). The comparison is between the involved limb of the patients with LE and a matched limb of the control
group. The matched limb of the control group was based on arm dominance. Control = 84 +/- 35 s, Involved = 53
+/- 37 s. * Indicates a significant difference between groups (P<.01).
Journal of Orthopaedic & Sports Physical Therapy
*
*
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FIGURE 7: Scapular Muscle Strength for Patients with LE. Data are means +/- standard deviations.
Abbreviations: LE, lateral epicondylalgia; LT, lower trapezius; MT, middle trapezius; SA, serratus anterior. Data:
LT Noninvolved = 122 +/- 25 N; LT Involved = 109 +/- 37 N; MT Noninvolved = 145 +/- 28 N; MT Involved = 138
+/- 38 N; SA Noninvolved = 204 +/- 51 N; SA Involved = 184 +/- 67 N * Indicates a significant difference between
groups (P<.01).
Journal of Orthopaedic & Sports Physical Therapy

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