Journal of Sport Rehabilitation, 2015, 24, 244 -251 http://dx.doi.org/10.1123/jsr.2013-0149 © 2015 Human Kinetics, Inc.
Original Research Report
Electromyography Activation Levels of the 3 Gluteus Medius Subdivisions During Manual Strength Testing Roald Otten, Johannes L. Tol, Per Holmich, and Rodney Whiteley Study Design: Cross-sectional. Context: Gluteus medius (GM) muscle dysfunction is associated with overuse injury. The GM is functionally composed of 3 separate subdivisions: anterior, middle, and posterior. Clinical assessment of the GM subdivisions is relevant to detect strength and activation deficits and guide specific rehabilitation programs. However, the optimal positions for assessing the strength and activation of these subdivisions are unknown. Objective: The first aim was to establish which strength-testing positions produce the highest surface electromyography (sEMG) activation levels of the individual GM subdivisions. The second aim was to evaluate differences in sEMG activation levels between the tested and contralateral (stabilizing) leg. Method: Twenty healthy physically active male subjects participated in this study. Muscle activity using sEMG was recorded for the GM subdivisions in 8 different strength-testing positions and analyzed using repeated-measures analysis of variance. Results: Significant differences between testing positions for all 3 GM subdivisions were found. There were significant differences between the tested and the contralateral anterior and middle GM subdivisions (P < .01). The posterior GM subdivision showed no significant difference (P = .154). Conclusion: Side-lying in neutral and side-lying with hip internal rotation are the 2 positions recommended to evaluate GM function and guide specific GM rehabilitation. Keywords: hip abductor, gluteus medius muscle parts, abductor strength The gluteus medius (GM) subdivisions are primary pelvic stabilizers and are essential for maintaining normal movement patterns of the pelvis and lower limb during daily activities1,2 and functional exercises.3 Dysfunction of these muscles is associated with lower-limb pathology such as patellofemoral pain syndrome,4 iliotibial band syndrome,5 and groin injuries.6,7 Furthermore, specific GM-strengthening programs are associated with favorable rehabilitation outcomes for these injuries.4,8–10 Given its association with these overuse injuries, detection of the GM dysfunction is relevant for daily clinical practice. The GM demonstrates 3 anatomically distinct subdivisions: anterior (GMA), middle (GMM), and posterior (GMP),11,12 which are thought to have functionally different roles. Several studies have shown that these 3 GM subdivisions have different activation patterns during different activities. O’Dwyer et al13 showed a variation in activation of the different subdivisions when altering thigh rotation, while O’Sullivan et al14 showed variation of activation in 3 different functional weight-bearingexercise positions. Semciw et al15 demonstrated variation The authors are with Aspetar—Qatar Orthopedic and Sports Medicine Hospital, Doha, Qatar. Address author correspondence to Roald Otten at [email protected].
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in activation levels of the 3 subdivisions during gait, as well as during 4 different clinical exercises. Improved knowledge of the activation patterns will enhance accuracy of diagnosis in GM dysfunction, as well as providing information helpful in optimizing exercise strategies. Previous work has shown similar values in both legs for hip-abduction-strength testing in healthy subjects, and it has been suggested that examining the uninjured side can provide information regarding the target strength in the case of a unilateral injury to the hip abductors.16 Activation levels of the contralateral leg during these movements and exercises are unknown. Clinically we had reports of fatigue in the stabilizing leg during both stance and non-weight-bearing exercises, suggesting to us that the nontested (ie, stabilizing) leg was being activated during strength testing, yet the literature (Semciw et al15) does not report this activation. An accurate assessment of GM strength will involve minimizing activation in this contralateral leg such that valid clinical implications can be drawn. Surface electromyography (sEMG) is a reliable method of recording these muscleactivation levels.17,18 The first aim of this study was to establish which strength-testing positions have the highest sEMG activation levels of the individual GM subdivisions. The second aim was to evaluate differences in activation levels between the tested and contralateral (stabilizing) legs.
sEMG of the Gluteus Medius 245
Methods Participants Twenty healthy physically active white, or Caucasian, male subjects (mean age 37 ± 5 y, median age 35.3 y) volunteered to participate in this study. All subjects had no recent (6 mo) history of back, pelvic, hip, or lowerextremity injury. Informed consent was obtained before participation. The study was approved by the Shafallah Medical Genetics Center ethical review board, and the study was conducted in accordance with the Declaration of Helsinki.
Design
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The study was a cross-sectional study.
Procedures Collection of sEMG data was performed with wireless sEMG (Delsys Trigno, Boston, MA). A gain of 1000 Hz and a bandwidth of 50 to 450 Hz was used. Before electrode placement, the subject’s skin was shaved and then cleaned with alcohol, in accordance with the SENIAM (Surface ElectroMyoGraphy for the NonInvasive Assessment of Muscles) guidelines.19 The dominant side was determined by asking the subject with which leg he would kick a ball, and this side was used as the strength-testing leg during the protocol. Rectangular electrodes measuring 37 × 26 × 15 mm (Delsys Trigno, Boston, MA) were placed on both the dominant and the nondominant side. Electrode location was based on the work by O’Sullivan et al,14 who describe a modified version of the SENIAM guideline based on previous EMG studies, anatomical dissection studies, and textbook illustrations. Specifically, the anterior GM electrode was placed 50% of the distance between the anterosuperior iliac spine and the greater trochanter. The middle GM electrode was placed 50% of the distance between the greater trochanter and the iliac crest. The posterior GM electrode was placed 33% of the distance between the posterior ilium and the greater trochanter. The posterior ilium landmark was established by the point marking 20% of the distance between the iliac crest and the L4–L5 spinous process interspace. These anatomical landmarks were marked with a surgical marker pen, and a second investigator checked these before electrode placement. All electrodes were placed by 1 investigator, aligned in the direction of fiber orientation, on every subdivision for every subject with the subject standing. Signal quality was confirmed by examination of the EMG output while applying manual resistance during active hip abduction in supine. Electrodes were checked for good placement and contact frequently throughout the testing procedure. Before the sEMG recording trials, all subjects performed a 5-minute warm-up on an exercise cycle (Technogym Excite Bike 700, Rome, Italy) on level 6 such that the cycle reported, in Watts, a reading of 150%
of body weight (in kg). For example, an 80-kg athlete warmed up at 120 W. Subjects were instructed to perform 3 maximal voluntary isometric contractions (MVICs) with the dominant leg, against a handheld dynamometer (Baseline 130 electronic push/pull dynamometer Model 12–0343, Fabrication Enterprises Inc, Elmsford, NY), to simulate clinical strength-testing procedures.20 During each MVIC the investigator gave vigorous but standardized verbal encouragement.21 The force reading from the handheld dynamometer was reported to the subject after each trial, but there was no feedback given regarding the EMG. After each MVIC the resting period was 10 seconds. Between test positions the subject had a resting period of 2 minutes. The sEMG recording was performed in 8 different strength-testing positions (Figure 1): • Supine with straight legs (SSL). • Supine with the contralateral leg flexed (SCLF): The medial malleolus of the contralateral leg is positioned at the same height as the joint line of the knee of the tested leg. • Side-lying with the hip joints in neutral position (SL0). • Side-lying with the tested leg in 20° of abduction (SL20): The 20° of abduction was verified using an inclinometer (Polycast Protractor #36, Empire, Mukwonago, WI, USA). • Side-lying with the hip of the tested leg maximally internally rotated (SLIR). • Side-lying with the hip of the tested leg maximally externally rotated (SLER). • Side-lying with the tested leg in full extension and external rotation (SLEXT+ER). • Side-lying in the clam position (SLclam): 45° of hip flexion and 90° of knee flexion, verified using a goniometer (Baseline, White Plains, NY, USA). In each position the subject stabilized by holding on to the bed. In the supine testing positions (positions 1 and 2) this was done by holding on to the sides of the bed with both hands, while in the other 6 (side-lying) positions the subject held on to the bed with the ipsilateral (to the leg being tested) hand, the other hand rested under the head of the subject. All testing was performed by 1 investigator, who had 3 years of clinical experience with handheld dynamometer strength testing. The order of testing was randomized using an Internet-based randomization tool.22
Data and Statistical Analyses Raw sEMG signals were imported into Spike2 software (Cambridge Electronic Design, Cambridge, England) and were visually inspected to ensure correct signal quality and exclusion of possible artifacts. For each GM subdivision and each MVIC, the root-mean-square signal amplitude was calculated and smoothed over 100 points. Subsequently, the mean for the time period of
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Figure 1 — Depiction of the 8 strength-testing positions. (A) Supine straight leg. (B) Supine contralateral leg flexed. (C) Sidelying 0°. (D) Side-lying 20°. (E) Side-lying internal rotation. (F) Side-lying external rotation. (G) Side-lying extension with external rotation. (H) Side-lying clam.
500 milliseconds surrounding the peak of the sEMG was calculated.23,24 For each muscle subdivision in each position, a mean was calculated for the 3 MVICs that were performed and used in further comparison. The highest sEMG observed for a given subdivision (irrespective of in which of the 8 test positions this occurred) was considered the MVIC for this subdivision, for this subject, from which all subsequent normalization was derived.25 That is to say that this highest activation level (in millivolts) was considered to be 100%, and all measurements referenced this value to express relative (percent) activation. Descriptive statistics of the normalized sEMG data were calculated, and the data were subjected to a repeated-measures analysis of variance (ANOVA) (SPSS 19, IBM, Armonk, NY). The main effects of position, side, and subdivision were examined. The Mauchley test of sphericity was employed, and where the assumption of
sphericity was violated, F ratios based on GreenhouseGeisser correction were used. Wherever a significant association was found, Bonferroni post hoc correction was applied. Statistical significance of P ≤ .05 was determined a priori. Effect sizes were calculated using partial eta-squared to determine the practical relevance of significant findings.
Results All 20 subjects completed the test protocol. The normalized sEMG activation data for both the tested and the contralateral (stabilizing) GM subdivisions in each position are presented in Table 1 and Figure 2. Mean normalized sEMG data for the tested leg show that for the GMA subdivision, 5 out of 8 positions (SSL, SCFL, SL0, SLER, and SLext+ER) have relatively high
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Table 1 sEMG Activation Levels for Each Gluteus Medius Subdivision, for Both the Tested and Stabilizing Legs, Mean ± SD Dominant
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GMA
Nondominant
GMM
GMP
GMA
GMM
GMP
SSL
79% ± 8%*
64% ± 15%
64% ± 16%*
46% ± 14%*
54% ± 16%
56% ± 12%*
SCLF
79% ± 12%*
64% ± 13%
68% ± 14%
50% ± 15%*
55% ± 15%
65% ± 11%
SL0
75% ± 12%*
76% ± 17%*
77% ± 19%*
50% ± 19%*
58% ± 18%*
58% ± 12%*
SL20
71% ± 11%*
64% ± 15%*
66% ± 16%*
47% ± 20%*
50% ± 13%*
52% ± 11%*
SLIR
69% ± 13%*
79% ± 14%*
76% ± 19%*
52% ± 18%*
58% ± 17%*
53% ± 16%*
SLER
75% ± 10%*
54% ± 16%
59% ± 19%
39% ± 15%*
51% ± 15%
61% ± 11%
SLext +ER
76% ± 14%*
54% ± 17%
55% ± 18%
42% ± 21%*
52% ± 18%
61% ± 13%
SLclam
32% ± 17%*
20% ± 10%*
37% ± 13%*
21% ± 10%*
40% ± 21%*
60% ± 19%*
Abbreviations: GMA, gluteus medius anterior; GMM, gluteus medius middle; GMP, gluteus medius posterior; SSL, supine straight legs; SCLF, supine contralateral leg flexed; SL0, side-lying 0°; SL20, side-lying 20°; SLIR, side-lying internal rotation; SLER, side-lying external rotation; SLext+ER, side-lying extension + external rotation; SLclam, side-lying clam. *Significant difference between sides (P ≤ .05).
activation levels (>75%). For both the GMM and GMP subdivisions there are only 2 positions (SL0 and SLIR) that have such high activation levels. When considering activation levels in the contralateral (stabilizing) leg, the GMA subdivision shows significant differences (higher activation) from the contralateral leg in all testing positions. For the GMM this is the case in 4 out of 8 positions (SL0, SL20, SLIR, and SLclam) and for the GMP in 5 out of 8 (SSL, SL0, SL20, SLIR, and SLclam). The repeated-measures ANOVA revealed an overall position effect for each GM subdivision (GMA F7,133 = 29.8, P < .01, η2 = .610; GMM F7,133 = 30.4, P < .01, η2 = .615; GMP F7,133 = 8.1, P < .01, η2 = .3). For the condition of side, there was an overall effect for the GMA and GMM, but not for the GMP (GMA F1,19 = 119.2, P < .01, η2 = .863; GMM F1,19 = 5.6, P = .029, η2 = .228; GMP F1,19 = 2.2, P = .154, η2 = .104). For each GM subdivision there was an overall interaction effect between position and side (GMA F4,75 = 5.8, P < .01, η2 = .235; GMM F4,80 = 9.8, P < .01, η2 = .341; GMP F4,80 = 19.9, P < .01, η2 = .512). The post hoc pairwise comparisons between the different testing positions are displayed in Table 2.
Discussion This was the first study to evaluate the activation of all 3 GM subdivisions during clinical strength testing. The activation of the 3 GM subdivisions varies both with testing position and muscle role—either as the tested muscle or the stabilizing muscle on the contralateral extremity. Our main finding was that SL0 and SLIR are the testing positions that show the highest activations for all GM subdivisions. These 2 positions are recommended for daily practice to evaluate GM function and specific GM strengthening. In the testing positions examined here, it was not possible to selectively activate a single subdivision of the GM. As SL0 and SLIR are, compared with the other
testing positions, exhibiting higher muscle-activation levels for all GM subdivisions, these 2 positions could be considered optimal for assessing the function of the entire GM muscle. The finding that the GM was more active in internal rotation than in external rotation corroborates the findings of Earl,26 who demonstrated that the GMA and GMM were significantly more active during combined abduction and internal rotation than during simple abduction or a combined abduction/external-rotation task. We suggest that if activation of all subdivisions of the GM is a clinical aim, these positions could be used in a strengthening program. We can speculate that this (external-rotation) position places the greater trochanter more posteriorly, therefore placing the GM subdivisions at a mechanical disadvantage when attempting to forcefully abduct. Potentially, activation of the tensor fascia latae is substituting in this position. Further research is suggested to elucidate the mechanisms of these differences that may influence clinical testing and exercise interventions. Previous research has documented symmetry in strength testing of each leg in the SCLF position in a cohort of professional footballers.16 Thorborg et al16 suggested that an injured player could therefore have the strength of the uninjured leg examined to determine strength targets for rehabilitation. If clinical implications are being drawn from a side-to-side strength difference for a given individual, it is crucial that the tested leg is indeed the limiting factor when measuring the strength a subject can produce. Alternatively, it could be that a lack of activation in the contralateral (stabilizing) leg is the limiting factor during a strength test, and the clinician inadvertently ascribes the result to weakness in the tested leg. The results presented here show the GMA to have significantly higher activation in this (SCLF) testing position in the tested leg (compared with the nontested, stabilizing leg); however, GMM and GMP show similar
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Figure 2 — Graphical depiction of the mean surface electromyography (sEMG) activation (in percent) levels along with the standard deviation for each gluteus medius subdivision, for both the tested and stabilizing leg. Abbreviations: MVIC, maximal voluntary isometric contraction; GMA, gluteus medius anterior; GMM, gluteus medius middle; GMP, gluteus medius posterior; SSL, supine straight legs; SCLF, supine contralateral leg flexed; SL0, side-lying 0°; SL20, side-lying 20°; SLIR, side-lying internal rotation; SLER, side-lying external rotation; SLext+ER, side-lying extension + external rotation; SLclam, side-lying clam.
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sEMG of the Gluteus Medius 249
Table 2 Differences Between Mean sEMG Activation Levels of the Different Testing Positions for Each Dominant Gluteus Medius Subdivision SCLF
SL0
SL20
SLIR
SLER
Slext+ER
Slclam
GMA SSL
0%
SCLF
4%
7%
10%
4%
3%
47%*
4%
7%
10%
4%
3%
47%*
4%
6%
0%
–1%
43%*
2%
–4%
–5%
40%*
–6%
–7%
37%*
–1%
43%*
SL0 SL20 SLIR SLER SLext+ER
44%*
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SSL
1%
SCLF
–12%* –13%*
SL0
0%
–15%*
–1%
–16%*
12%
–3%
SL20
–15%*
SLIR
10%
10%
44%*
9%
10%
43%*
22%*
22%*
56%*
10%
11%
44%*
26%*
26%*
60%*
34%
34%*
SLER SLext+ER
34%*
GMP SSL SCLF SL0
–3%
–12%*
–1%
–12%
2%
–9%
9%
13%
30%*
11%*
0%
18%*
22%*
39%*
–11%
7%
11%
28%*
18%*
21%*
39%*
3%
21%*
–9%
SL20 SLIR SLER SLxt+ER
6%
9%
27%*
18%*
Abbreviations: GMA, gluteus medius anterior; GMM, gluteus medius middle; GMP, gluteus medius posterior; SSL, supine straight legs; SCLF, supine contralateral leg flexed; SL0, side-lying 0°; SL20, side-lying 20°; SLIR, side-lying internal rotation; SLER, side-lying external rotation; SLext+ER, sidelying extension + external rotation; SLclam, side-lying clam. *Significant difference between positions (P ≤ .05).
activation levels bilaterally. The SL0 and SLIR positions (the positions with the high activation levels in all tested GM subdivisions) are the only positions that had significantly higher differences from the contralateral (stabilizing) leg in all GM subdivisions. We therefore recommend these positions for clinical testing of GM strength. We note that none of the testing positions described successfully showed a high activation of all subdivisions in one leg with concurrent minimal (close to zero) activation in the other. We suggest that for this reason, none of the documented testing positions are truly examining 1 leg in isolation, and rather both legs are being activated, albeit at different levels, during these tests. We note, however, that it may be possible to infer side-to-side differences in strength by performing a strength test that shows high side-to-side difference in sEMG activation levels of the tested and nontested legs (see Table 2).
The SLclam position is often used by clinicians as a testing or exercise position for the GM muscle.27 We were interested to discover that the SLclam position shows very low activation levels for both the tested and the stabilizing leg, with exception of the contralateral GMP subdivision (60% activation). This is consistent with a recent study done by Willcox and Burden,28 who looked at GM activation levels while subjects performed unloaded, through-range clam movements and found similar low activation levels for the tested leg. It is suggested that activation levels of approximately 60% or greater are required to provide a hypertrophic training stimulus.29 As such, the other positions examined here may be more suitable for this purpose. Conversely, in early stages of rehabilitation where lower loads of activation are sought, the SLclam can be an appropriate introductory exercise. Speculating on the mechanism of the lower activation
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levels seen, we suggest that the SLclam position is both a shorter lever exercise (with resistance placed at the knee rather than the ankle) and potentially activates the GM preferentially. Further research is suggested to clarify this.
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Limitations This research used healthy, physically active male subjects. The findings are only applicable for this group, as the anatomy and muscle-activation patterns of the pelvis and groin are seen to vary according to gender.30,31 Future research is suggested to determine if these findings are also applicable for other groups, for example, females, injured subjects, or the elderly. Measurement using sEMG is influenced by factors such as thickness of tissue layers, crosstalk from nearby muscles, and electrode shifting.32 We attempted to minimize these factors by adhering to SENIAM guidelines for skin preparation, as well as employing isometric muscle testing, which minimizes the possibility of relative movement of the electrodes.
Conclusion SL0 and SLIR are the most suitable positions to test the strength of all 3 GM subdivisions in healthy male subjects. Both positions show the highest sEMG activation levels for all the GM subdivisions and have the advantage of having a significant difference in activation levels from the contralateral (stabilizing) leg. These finding should be considered when evaluating GM function or performing specific GM strengthening. Acknowledgments Ethical approval was granted by the Shafallah Medical Genetics Center (IRB-project number 2012–08).
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Original Research Report
Electromyography Activation Levels of the 3 Gluteus Medius Subdivisions During Manual Strength Testing Roald Otten, Johannes L. Tol, Per Holmich, and Rodney Whiteley Study Design: Cross-sectional. Context: Gluteus medius (GM) muscle dysfunction is associated with overuse injury. The GM is functionally composed of 3 separate subdivisions: anterior, middle, and posterior. Clinical assessment of the GM subdivisions is relevant to detect strength and activation deficits and guide specific rehabilitation programs. However, the optimal positions for assessing the strength and activation of these subdivisions are unknown. Objective: The first aim was to establish which strength-testing positions produce the highest surface electromyography (sEMG) activation levels of the individual GM subdivisions. The second aim was to evaluate differences in sEMG activation levels between the tested and contralateral (stabilizing) leg. Method: Twenty healthy physically active male subjects participated in this study. Muscle activity using sEMG was recorded for the GM subdivisions in 8 different strength-testing positions and analyzed using repeated-measures analysis of variance. Results: Significant differences between testing positions for all 3 GM subdivisions were found. There were significant differences between the tested and the contralateral anterior and middle GM subdivisions (P < .01). The posterior GM subdivision showed no significant difference (P = .154). Conclusion: Side-lying in neutral and side-lying with hip internal rotation are the 2 positions recommended to evaluate GM function and guide specific GM rehabilitation. Keywords: hip abductor, gluteus medius muscle parts, abductor strength The gluteus medius (GM) subdivisions are primary pelvic stabilizers and are essential for maintaining normal movement patterns of the pelvis and lower limb during daily activities1,2 and functional exercises.3 Dysfunction of these muscles is associated with lower-limb pathology such as patellofemoral pain syndrome,4 iliotibial band syndrome,5 and groin injuries.6,7 Furthermore, specific GM-strengthening programs are associated with favorable rehabilitation outcomes for these injuries.4,8–10 Given its association with these overuse injuries, detection of the GM dysfunction is relevant for daily clinical practice. The GM demonstrates 3 anatomically distinct subdivisions: anterior (GMA), middle (GMM), and posterior (GMP),11,12 which are thought to have functionally different roles. Several studies have shown that these 3 GM subdivisions have different activation patterns during different activities. O’Dwyer et al13 showed a variation in activation of the different subdivisions when altering thigh rotation, while O’Sullivan et al14 showed variation of activation in 3 different functional weight-bearingexercise positions. Semciw et al15 demonstrated variation The authors are with Aspetar—Qatar Orthopedic and Sports Medicine Hospital, Doha, Qatar. Address author correspondence to Roald Otten at [email protected].
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in activation levels of the 3 subdivisions during gait, as well as during 4 different clinical exercises. Improved knowledge of the activation patterns will enhance accuracy of diagnosis in GM dysfunction, as well as providing information helpful in optimizing exercise strategies. Previous work has shown similar values in both legs for hip-abduction-strength testing in healthy subjects, and it has been suggested that examining the uninjured side can provide information regarding the target strength in the case of a unilateral injury to the hip abductors.16 Activation levels of the contralateral leg during these movements and exercises are unknown. Clinically we had reports of fatigue in the stabilizing leg during both stance and non-weight-bearing exercises, suggesting to us that the nontested (ie, stabilizing) leg was being activated during strength testing, yet the literature (Semciw et al15) does not report this activation. An accurate assessment of GM strength will involve minimizing activation in this contralateral leg such that valid clinical implications can be drawn. Surface electromyography (sEMG) is a reliable method of recording these muscleactivation levels.17,18 The first aim of this study was to establish which strength-testing positions have the highest sEMG activation levels of the individual GM subdivisions. The second aim was to evaluate differences in activation levels between the tested and contralateral (stabilizing) legs.
sEMG of the Gluteus Medius 245
Methods Participants Twenty healthy physically active white, or Caucasian, male subjects (mean age 37 ± 5 y, median age 35.3 y) volunteered to participate in this study. All subjects had no recent (6 mo) history of back, pelvic, hip, or lowerextremity injury. Informed consent was obtained before participation. The study was approved by the Shafallah Medical Genetics Center ethical review board, and the study was conducted in accordance with the Declaration of Helsinki.
Design
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The study was a cross-sectional study.
Procedures Collection of sEMG data was performed with wireless sEMG (Delsys Trigno, Boston, MA). A gain of 1000 Hz and a bandwidth of 50 to 450 Hz was used. Before electrode placement, the subject’s skin was shaved and then cleaned with alcohol, in accordance with the SENIAM (Surface ElectroMyoGraphy for the NonInvasive Assessment of Muscles) guidelines.19 The dominant side was determined by asking the subject with which leg he would kick a ball, and this side was used as the strength-testing leg during the protocol. Rectangular electrodes measuring 37 × 26 × 15 mm (Delsys Trigno, Boston, MA) were placed on both the dominant and the nondominant side. Electrode location was based on the work by O’Sullivan et al,14 who describe a modified version of the SENIAM guideline based on previous EMG studies, anatomical dissection studies, and textbook illustrations. Specifically, the anterior GM electrode was placed 50% of the distance between the anterosuperior iliac spine and the greater trochanter. The middle GM electrode was placed 50% of the distance between the greater trochanter and the iliac crest. The posterior GM electrode was placed 33% of the distance between the posterior ilium and the greater trochanter. The posterior ilium landmark was established by the point marking 20% of the distance between the iliac crest and the L4–L5 spinous process interspace. These anatomical landmarks were marked with a surgical marker pen, and a second investigator checked these before electrode placement. All electrodes were placed by 1 investigator, aligned in the direction of fiber orientation, on every subdivision for every subject with the subject standing. Signal quality was confirmed by examination of the EMG output while applying manual resistance during active hip abduction in supine. Electrodes were checked for good placement and contact frequently throughout the testing procedure. Before the sEMG recording trials, all subjects performed a 5-minute warm-up on an exercise cycle (Technogym Excite Bike 700, Rome, Italy) on level 6 such that the cycle reported, in Watts, a reading of 150%
of body weight (in kg). For example, an 80-kg athlete warmed up at 120 W. Subjects were instructed to perform 3 maximal voluntary isometric contractions (MVICs) with the dominant leg, against a handheld dynamometer (Baseline 130 electronic push/pull dynamometer Model 12–0343, Fabrication Enterprises Inc, Elmsford, NY), to simulate clinical strength-testing procedures.20 During each MVIC the investigator gave vigorous but standardized verbal encouragement.21 The force reading from the handheld dynamometer was reported to the subject after each trial, but there was no feedback given regarding the EMG. After each MVIC the resting period was 10 seconds. Between test positions the subject had a resting period of 2 minutes. The sEMG recording was performed in 8 different strength-testing positions (Figure 1): • Supine with straight legs (SSL). • Supine with the contralateral leg flexed (SCLF): The medial malleolus of the contralateral leg is positioned at the same height as the joint line of the knee of the tested leg. • Side-lying with the hip joints in neutral position (SL0). • Side-lying with the tested leg in 20° of abduction (SL20): The 20° of abduction was verified using an inclinometer (Polycast Protractor #36, Empire, Mukwonago, WI, USA). • Side-lying with the hip of the tested leg maximally internally rotated (SLIR). • Side-lying with the hip of the tested leg maximally externally rotated (SLER). • Side-lying with the tested leg in full extension and external rotation (SLEXT+ER). • Side-lying in the clam position (SLclam): 45° of hip flexion and 90° of knee flexion, verified using a goniometer (Baseline, White Plains, NY, USA). In each position the subject stabilized by holding on to the bed. In the supine testing positions (positions 1 and 2) this was done by holding on to the sides of the bed with both hands, while in the other 6 (side-lying) positions the subject held on to the bed with the ipsilateral (to the leg being tested) hand, the other hand rested under the head of the subject. All testing was performed by 1 investigator, who had 3 years of clinical experience with handheld dynamometer strength testing. The order of testing was randomized using an Internet-based randomization tool.22
Data and Statistical Analyses Raw sEMG signals were imported into Spike2 software (Cambridge Electronic Design, Cambridge, England) and were visually inspected to ensure correct signal quality and exclusion of possible artifacts. For each GM subdivision and each MVIC, the root-mean-square signal amplitude was calculated and smoothed over 100 points. Subsequently, the mean for the time period of
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Figure 1 — Depiction of the 8 strength-testing positions. (A) Supine straight leg. (B) Supine contralateral leg flexed. (C) Sidelying 0°. (D) Side-lying 20°. (E) Side-lying internal rotation. (F) Side-lying external rotation. (G) Side-lying extension with external rotation. (H) Side-lying clam.
500 milliseconds surrounding the peak of the sEMG was calculated.23,24 For each muscle subdivision in each position, a mean was calculated for the 3 MVICs that were performed and used in further comparison. The highest sEMG observed for a given subdivision (irrespective of in which of the 8 test positions this occurred) was considered the MVIC for this subdivision, for this subject, from which all subsequent normalization was derived.25 That is to say that this highest activation level (in millivolts) was considered to be 100%, and all measurements referenced this value to express relative (percent) activation. Descriptive statistics of the normalized sEMG data were calculated, and the data were subjected to a repeated-measures analysis of variance (ANOVA) (SPSS 19, IBM, Armonk, NY). The main effects of position, side, and subdivision were examined. The Mauchley test of sphericity was employed, and where the assumption of
sphericity was violated, F ratios based on GreenhouseGeisser correction were used. Wherever a significant association was found, Bonferroni post hoc correction was applied. Statistical significance of P ≤ .05 was determined a priori. Effect sizes were calculated using partial eta-squared to determine the practical relevance of significant findings.
Results All 20 subjects completed the test protocol. The normalized sEMG activation data for both the tested and the contralateral (stabilizing) GM subdivisions in each position are presented in Table 1 and Figure 2. Mean normalized sEMG data for the tested leg show that for the GMA subdivision, 5 out of 8 positions (SSL, SCFL, SL0, SLER, and SLext+ER) have relatively high
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Table 1 sEMG Activation Levels for Each Gluteus Medius Subdivision, for Both the Tested and Stabilizing Legs, Mean ± SD Dominant
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GMA
Nondominant
GMM
GMP
GMA
GMM
GMP
SSL
79% ± 8%*
64% ± 15%
64% ± 16%*
46% ± 14%*
54% ± 16%
56% ± 12%*
SCLF
79% ± 12%*
64% ± 13%
68% ± 14%
50% ± 15%*
55% ± 15%
65% ± 11%
SL0
75% ± 12%*
76% ± 17%*
77% ± 19%*
50% ± 19%*
58% ± 18%*
58% ± 12%*
SL20
71% ± 11%*
64% ± 15%*
66% ± 16%*
47% ± 20%*
50% ± 13%*
52% ± 11%*
SLIR
69% ± 13%*
79% ± 14%*
76% ± 19%*
52% ± 18%*
58% ± 17%*
53% ± 16%*
SLER
75% ± 10%*
54% ± 16%
59% ± 19%
39% ± 15%*
51% ± 15%
61% ± 11%
SLext +ER
76% ± 14%*
54% ± 17%
55% ± 18%
42% ± 21%*
52% ± 18%
61% ± 13%
SLclam
32% ± 17%*
20% ± 10%*
37% ± 13%*
21% ± 10%*
40% ± 21%*
60% ± 19%*
Abbreviations: GMA, gluteus medius anterior; GMM, gluteus medius middle; GMP, gluteus medius posterior; SSL, supine straight legs; SCLF, supine contralateral leg flexed; SL0, side-lying 0°; SL20, side-lying 20°; SLIR, side-lying internal rotation; SLER, side-lying external rotation; SLext+ER, side-lying extension + external rotation; SLclam, side-lying clam. *Significant difference between sides (P ≤ .05).
activation levels (>75%). For both the GMM and GMP subdivisions there are only 2 positions (SL0 and SLIR) that have such high activation levels. When considering activation levels in the contralateral (stabilizing) leg, the GMA subdivision shows significant differences (higher activation) from the contralateral leg in all testing positions. For the GMM this is the case in 4 out of 8 positions (SL0, SL20, SLIR, and SLclam) and for the GMP in 5 out of 8 (SSL, SL0, SL20, SLIR, and SLclam). The repeated-measures ANOVA revealed an overall position effect for each GM subdivision (GMA F7,133 = 29.8, P < .01, η2 = .610; GMM F7,133 = 30.4, P < .01, η2 = .615; GMP F7,133 = 8.1, P < .01, η2 = .3). For the condition of side, there was an overall effect for the GMA and GMM, but not for the GMP (GMA F1,19 = 119.2, P < .01, η2 = .863; GMM F1,19 = 5.6, P = .029, η2 = .228; GMP F1,19 = 2.2, P = .154, η2 = .104). For each GM subdivision there was an overall interaction effect between position and side (GMA F4,75 = 5.8, P < .01, η2 = .235; GMM F4,80 = 9.8, P < .01, η2 = .341; GMP F4,80 = 19.9, P < .01, η2 = .512). The post hoc pairwise comparisons between the different testing positions are displayed in Table 2.
Discussion This was the first study to evaluate the activation of all 3 GM subdivisions during clinical strength testing. The activation of the 3 GM subdivisions varies both with testing position and muscle role—either as the tested muscle or the stabilizing muscle on the contralateral extremity. Our main finding was that SL0 and SLIR are the testing positions that show the highest activations for all GM subdivisions. These 2 positions are recommended for daily practice to evaluate GM function and specific GM strengthening. In the testing positions examined here, it was not possible to selectively activate a single subdivision of the GM. As SL0 and SLIR are, compared with the other
testing positions, exhibiting higher muscle-activation levels for all GM subdivisions, these 2 positions could be considered optimal for assessing the function of the entire GM muscle. The finding that the GM was more active in internal rotation than in external rotation corroborates the findings of Earl,26 who demonstrated that the GMA and GMM were significantly more active during combined abduction and internal rotation than during simple abduction or a combined abduction/external-rotation task. We suggest that if activation of all subdivisions of the GM is a clinical aim, these positions could be used in a strengthening program. We can speculate that this (external-rotation) position places the greater trochanter more posteriorly, therefore placing the GM subdivisions at a mechanical disadvantage when attempting to forcefully abduct. Potentially, activation of the tensor fascia latae is substituting in this position. Further research is suggested to elucidate the mechanisms of these differences that may influence clinical testing and exercise interventions. Previous research has documented symmetry in strength testing of each leg in the SCLF position in a cohort of professional footballers.16 Thorborg et al16 suggested that an injured player could therefore have the strength of the uninjured leg examined to determine strength targets for rehabilitation. If clinical implications are being drawn from a side-to-side strength difference for a given individual, it is crucial that the tested leg is indeed the limiting factor when measuring the strength a subject can produce. Alternatively, it could be that a lack of activation in the contralateral (stabilizing) leg is the limiting factor during a strength test, and the clinician inadvertently ascribes the result to weakness in the tested leg. The results presented here show the GMA to have significantly higher activation in this (SCLF) testing position in the tested leg (compared with the nontested, stabilizing leg); however, GMM and GMP show similar
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Figure 2 — Graphical depiction of the mean surface electromyography (sEMG) activation (in percent) levels along with the standard deviation for each gluteus medius subdivision, for both the tested and stabilizing leg. Abbreviations: MVIC, maximal voluntary isometric contraction; GMA, gluteus medius anterior; GMM, gluteus medius middle; GMP, gluteus medius posterior; SSL, supine straight legs; SCLF, supine contralateral leg flexed; SL0, side-lying 0°; SL20, side-lying 20°; SLIR, side-lying internal rotation; SLER, side-lying external rotation; SLext+ER, side-lying extension + external rotation; SLclam, side-lying clam.
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sEMG of the Gluteus Medius 249
Table 2 Differences Between Mean sEMG Activation Levels of the Different Testing Positions for Each Dominant Gluteus Medius Subdivision SCLF
SL0
SL20
SLIR
SLER
Slext+ER
Slclam
GMA SSL
0%
SCLF
4%
7%
10%
4%
3%
47%*
4%
7%
10%
4%
3%
47%*
4%
6%
0%
–1%
43%*
2%
–4%
–5%
40%*
–6%
–7%
37%*
–1%
43%*
SL0 SL20 SLIR SLER SLext+ER
44%*
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SSL
1%
SCLF
–12%* –13%*
SL0
0%
–15%*
–1%
–16%*
12%
–3%
SL20
–15%*
SLIR
10%
10%
44%*
9%
10%
43%*
22%*
22%*
56%*
10%
11%
44%*
26%*
26%*
60%*
34%
34%*
SLER SLext+ER
34%*
GMP SSL SCLF SL0
–3%
–12%*
–1%
–12%
2%
–9%
9%
13%
30%*
11%*
0%
18%*
22%*
39%*
–11%
7%
11%
28%*
18%*
21%*
39%*
3%
21%*
–9%
SL20 SLIR SLER SLxt+ER
6%
9%
27%*
18%*
Abbreviations: GMA, gluteus medius anterior; GMM, gluteus medius middle; GMP, gluteus medius posterior; SSL, supine straight legs; SCLF, supine contralateral leg flexed; SL0, side-lying 0°; SL20, side-lying 20°; SLIR, side-lying internal rotation; SLER, side-lying external rotation; SLext+ER, sidelying extension + external rotation; SLclam, side-lying clam. *Significant difference between positions (P ≤ .05).
activation levels bilaterally. The SL0 and SLIR positions (the positions with the high activation levels in all tested GM subdivisions) are the only positions that had significantly higher differences from the contralateral (stabilizing) leg in all GM subdivisions. We therefore recommend these positions for clinical testing of GM strength. We note that none of the testing positions described successfully showed a high activation of all subdivisions in one leg with concurrent minimal (close to zero) activation in the other. We suggest that for this reason, none of the documented testing positions are truly examining 1 leg in isolation, and rather both legs are being activated, albeit at different levels, during these tests. We note, however, that it may be possible to infer side-to-side differences in strength by performing a strength test that shows high side-to-side difference in sEMG activation levels of the tested and nontested legs (see Table 2).
The SLclam position is often used by clinicians as a testing or exercise position for the GM muscle.27 We were interested to discover that the SLclam position shows very low activation levels for both the tested and the stabilizing leg, with exception of the contralateral GMP subdivision (60% activation). This is consistent with a recent study done by Willcox and Burden,28 who looked at GM activation levels while subjects performed unloaded, through-range clam movements and found similar low activation levels for the tested leg. It is suggested that activation levels of approximately 60% or greater are required to provide a hypertrophic training stimulus.29 As such, the other positions examined here may be more suitable for this purpose. Conversely, in early stages of rehabilitation where lower loads of activation are sought, the SLclam can be an appropriate introductory exercise. Speculating on the mechanism of the lower activation
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levels seen, we suggest that the SLclam position is both a shorter lever exercise (with resistance placed at the knee rather than the ankle) and potentially activates the GM preferentially. Further research is suggested to clarify this.
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Limitations This research used healthy, physically active male subjects. The findings are only applicable for this group, as the anatomy and muscle-activation patterns of the pelvis and groin are seen to vary according to gender.30,31 Future research is suggested to determine if these findings are also applicable for other groups, for example, females, injured subjects, or the elderly. Measurement using sEMG is influenced by factors such as thickness of tissue layers, crosstalk from nearby muscles, and electrode shifting.32 We attempted to minimize these factors by adhering to SENIAM guidelines for skin preparation, as well as employing isometric muscle testing, which minimizes the possibility of relative movement of the electrodes.
Conclusion SL0 and SLIR are the most suitable positions to test the strength of all 3 GM subdivisions in healthy male subjects. Both positions show the highest sEMG activation levels for all the GM subdivisions and have the advantage of having a significant difference in activation levels from the contralateral (stabilizing) leg. These finding should be considered when evaluating GM function or performing specific GM strengthening. Acknowledgments Ethical approval was granted by the Shafallah Medical Genetics Center (IRB-project number 2012–08).
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