Central Activation Ratio Is a Reliable Measure for Gluteal Neuromuscular Function

in Journal of Sport Rehabilitation

Context: Central activation ratio (CAR) is a common outcome measure used to quantify gross neuromuscular function of the quadriceps using the superimposed burst technique, yet this outcome measure has not been validated in the gluteal musculature. Objective: To quantify gluteus medius (GMed) and gluteus maximus (GMax) CAR in a healthy population and evaluate its validity and reliability over a 1-week period. Design: Descriptive. Setting: Laboratory. Patients or Other Participants: A total of 20 healthy participants (9 males and 11 females; age 22.2 [1.4] y, height 173.4 [11.1] cm, mass 84.8 [25.8] kg) were enrolled in this study. Interventions: Participants were assessed at 2 sessions, separated by 1 week. Progressive electrical stimuli (25%, 50%, 75%, and 100%) were delivered to the GMed and GMax at rest, and 100% stimuli were delivered during progressive hip abduction and extension contractions (25%, 50%, 75%, and 100% maximal voluntary isometric contraction). Main Outcome Measures: GMed and GMax CAR, and hip abduction and hip extension maximal voluntary isometric contraction torque. Line of best fit and coefficient of determination (r2) were used to assess the relationship between torque output and CAR at varying levels of stimuli. Intraclass correlation coefficients, ICCs(3,k), were used to assess the between-session reliability. Results: GMed CAR was 96.1% (3.4%) and 96.6% (3.2%), on visits 1 and 2, respectively, whereas GMax CAR was 86.5% (7.5%) and 87.2% (10.7%) over the 2 sessions. A third-order polynomial demonstrated the best line of fit between varying superimposed burst intensities at rest for both GMed (r2 = .156) and GMax (r2 = .602). Linear relationships were observed in the CAR during progressive contractions with a maximal superimposed burst, GMed (r2 = .409) and GMax (r2 = .639). Between-session reliability was excellent for GMed CAR, ICC(3,k) = .911, and moderate for GMax CAR, ICC(3,k) = .704. Conclusion: CAR appears to be an acceptable measure of GMed and GMax neuromuscular function in healthy individuals. Gluteal CAR measurements are reliable measures over a 1-week test period.

The gluteus medius (GMed) and gluteus maximus (GMax) muscles play a vital role in maintaining the horizontal position of the pelvis,1 frontal plane lower-extremity movements,2,3 and the torso’s upright position during normal gait patterns.4 Therefore, it is important that these 2 muscle groups stay properly activated and are being used appropriately. However, gluteal weakness is a common impairment seen in a variety of lower-extremity conditions, including, but not limited to, patients with a history of low back pain5 and patellofemoral pain,6 and anterior cruciate ligament–reconstructed patients.7 Poor neuromuscular function of the gluteal muscles has also been related to altered frontal hip and knee plane motion2,3 and decreased subjective knee function.8 Due to their relationship between gluteal weakness and poor subjective and objective functional measurements, optimizing gluteal function is a cornerstone of conservative treatment9 and injury prevention programs.10

Although strength represents the most common way to assess muscular function, it has some limitations at providing a muscle’s optimal neuromuscular capabilities. Emerging evidence has suggested that additional measures, such as the superimposed burst (SIB) technique (SIBT), may provide more unique information at understanding complete muscle function.11,12 The SIBT has been identified to have stronger relationship to objective measures, such as landing biomechanics and gait kinetics, than strength assessments alone.11,12 One outcome that has been used to evaluate muscle function is the central activation ratio (CAR), assessed by the SIBT. CAR has previously been utilized in research as a way to measure the volitional activation of the quadriceps in a variety of pathologies.1315 The CAR is a ratio between the volitional muscle contraction and muscle activation elicited by an exogenous electrical stimulus.13 SIBT is the application of an electrical stimulation during a maximal voluntary isometric contraction (MVIC) that, in theory, activates the remaining motor units that the patient was unable to do so during their MVIC.14 CAR, assessed by the SIBT, is a valid and reliable measurement at assessing quadriceps muscle function in healthy16 and pathological populations.15,17 This provides researchers a way to measure muscle inhibition, which is an underlying mechanism that may limit an individual’s ability to use their muscle to its maximum capabilities.15

Although a variety of lower-extremity pathologies have been assessed with the CAR, the research is mostly limited to the quadriceps.13,14,17,18 Expanding the use of this measurement on other superficial muscle groups provides the ability to assess if activation failure is present in other muscles during lower-extremity conditions. Due to the importance of the gluteal muscles during daily activities and evidence of their weakness in a variety of conditions,19 it is important to gain a more complete assessment of their neuromuscular function. This knowledge is essential to assess the effectiveness of interventions that target the gluteal muscles; however before this can happen, the validity and reliability of this measure must be established.

Therefore, the purpose of this study was to determine the validity and between-session reliability of gluteal CAR measures as assessed by the SIB. We also assessed the participant discomfort during CAR of both gluteal muscles. We hypothesize that the CAR is a valid and reliable method to assess gluteal muscle activity. In addition, we hypothesized that there will be a linear relationship between progression of muscular contractions with maximal SIB on the CAR of the gluteal muscles. We also hypothesized that participant discomfort would be comparable with discomfort during SIB of the quadriceps.

Methods

Participants

In total, 20 healthy volunteers were recruited from the University of Toledo and local community (9 males and 11 females; age 22.2 [1.4] y, height 173.4 [11.1] cm, mass 84.8 [25.8] kg) and were enrolled in this descriptive laboratory study. Participants were screened for inclusion and exclusion criteria (Table 1). The study was approved by the University of Toledo Institutional Review Board, and all participants completed the informed consent prior to study enrollment.

Table 1

Participants’ Inclusion/Exclusion Criteria

Inclusion
 • Healthy adults aged between 18 and 35 y
 • Physically active 2–3x per week
Exclusion
 • Previous surgery to lower-extremity or back
 • Previous injury to the lower-extremity or back in the last 6 mo
 • Current lower-extremity muscle soreness from a workout in the previous 24–48 h
 • History of neuropathy
 • Biomedical devices (pacemaker, defibrillators, etc)
 • Muscle abnormalities
 • Currently pregnant
 • Hypersensitivity to electrical stimulation
 • Active infection over the thigh or hip muscles

Procedures

Enrolled participants reported to the research laboratory for 2 testing sessions, separated by 1 week. A 2 × 2 block randomization was completed prior to the start of the study for order of muscles being tested, which was maintained between both sessions. Dominant limb was selected for testing, which was defined as the leg the participant would kick a ball with.

Then, participants were prepared with electrodes over the test muscles. GMed testing included placing of two 2 × 3.5-in self-adhesive electrodes (Axelgaard, Fallbrook, CA) on the muscle, with one electrode just inferior to the iliac crest and the other electrode just superior to the greater trochanter. Participants completed hip abduction strength testing in a standing position in a Biodex System 4 Pro dynamometer (Biodex Medical Systems, Inc, Shirley, NY), with the axis of rotation aligned to their anterior superior iliac spine and the dynamometer arm secured just superior to the lateral femoral condyle. This position was selected to minimize the effect of gravity during testing. The dynamometer chair was positioned at the height of the participant’s hips, and a bolster was positioned between the participant and chair to stabilize trunk motion (Figure 1). During testing, participants were instructed to place their arms across their chest, maintain an upright position, and provide maximal effort.

Figure 1
Figure 1

—Participant setup for gluteus medius testing.

Citation: Journal of Sport Rehabilitation 29, 7; 10.1123/jsr.2019-0243

For the GMax testing, two 2 × 3.5-in self-adhesive electrodes were placed on the muscle belly, one just superior to the gluteal fold and the other just inferior to the posterior superior iliac spine. Participants were prone, with their hips and knee flexed at 90° for hip extension testing. The axis of rotation was aligned with participant’s greater trochanter, and the dynamometer arm was secured just proximal to the popliteal fossa. Strapping was placed over the participant’s back to minimize excessive movement during the task, and participants were instructed to place their hands above them for testing (Figure 2).

Figure 2
Figure 2

—Participant setup for gluteus maximus testing.

Citation: Journal of Sport Rehabilitation 29, 7; 10.1123/jsr.2019-0243

The dynamometer was used to measure hip extension and hip abduction force. Force data were acquired using a 16-bit acquisition system at 125 Hz (MP150; BIOPAC Systems, Inc, Santa Barbara, CA).17 A series of exogenous electrical stimuli were delivered to the respective muscles using a Grass Stimulator S48 (Grass Technologies, West Warwick, RI) and Stimulus Isolation Unit (Grass Stimulator; Grass Technologies, West Warwick, RI). The isolation unit delivered a 100-millisecond train of 10 square-wave pulses at an intensity of 125 V (pulse duration: 600 μs and frequency: 100 Hz).20 The SIB stimulus was manually administered during testing when a steady real-time torque output plateau was observed by the investigator.

Participants were acclimated to the task by completing a series of submaximal contractions at 25%, 50%, and 75% of their perceived MVIC.17 Participants were instructed to perform the task by ramping up to the submaximal contraction and maintain that intensity for 3 to 5 seconds. Following the gradual warm-up, participants completed 2 maximal contractions, while being provided with strong verbal and visual feedback on a monitor. Once the participant felt comfortable with MVIC task, they performed MVIC trials with the SIB. The SIB was delivered in increments of 25% of the maximal testing voltage of 125 V until the maximal stimulus was delivered.21 Two trials of submaximal stimuli (25%, 50%, and 75%) and 3 maximal stimuli trials (100%) were collected. Following the 3 maximal stimuli trials, participants completed a self-reported pain assessment they experienced during testing using a visual analog scale (VAS). The 10 cm line was anchored with “no pain” and “worst pain imaginable” and is reliable and valid measure of pain.22 Participants then completed graded stimuli at rest, which included 2 trials at 25%, 50%, 75%, and 100% stimuli. Following graded stimuli at rest trials, participants completed progressive contractions (25%, 50%, 75%, and 100%) with a 100% stimulus, with 2 trials completed for each. All testing procedures were completed for both hip extension and hip abduction, with a 1-minute break between all trials and a 5-minute break between each muscle of interest. This concluded the first testing session, and participants scheduled a second testing session 1 week later.

Participants returned to the laboratory for their second testing session and completed the gradual MVIC warm-up similar to the initial session. Then, they completed 3 MVICs trials with the 100% SIB for both the GMed and GMax. The order of testing each muscle was identical to their initial visit. Pain was assessed at the completion of testing for each muscle as described previously.

Data Analysis

All force data were normalized to body mass and converted to torque (in newton meters/kilogram). The average of the trials was used for all analyses. Peak SIB torque output was also calculated with the same approach. CAR was calculated by using a 100-millisecond epoch of the maximal and submaximal torque output immediately prior to delivery of SIB stimuli and the combination of the torque and SIB output from the stimulus, multiplied by 100, as previously reported:

CAR=Torque output(Torque output+SIB)×100.
The CAR is presented as a percentage of complete activation, ranging from 0% to 100%, with a greater number representing a greater percentage of muscle activation. VAS was scored by measuring the distance (in centimeters) between the “no pain” anchor and the vertical line placed by the participant.

Statistical Analysis

Descriptive statistics were performed for participants’ demographics and both testing session’s CAR, MVIC, SIB output, and VAS scores for the GMed and GMax. Validity was assessed by evaluating 2 separate relationships of variables by plotting the line of best fit via regressions to calculate the coefficient of determination.23 The first relationship was comparing the graded stimuli at rest with the torque output to evaluate complete gluteal motor unit recruitment. The second relationship was comparing the relationship between the maximal stimulus during the progressive contractions on gluteal CAR measurements to assess CAR and voluntary effort. Separate Pearson correlation coefficients were performed to identify correlations between the 2 assessments of each GMed and GMax function (MVIC and CAR) during the initial testing sessions. Correlations were classified as weak (<.4), moderate (.4–.7), and strong (>.7).24 Reliability of the gluteal CAR was only assessed at the 100% SIB during the MVIC trials between the 2 days and was assessed by intraclass correlation coefficients, ICCs(3,k) and classified as poor (<.5), moderate (.5–.75), good (.75–.90), and excellent (>.90).25 Paired t tests were also used to compare averages in CAR, MVIC, SIB torque, and VAS scores between the 2 sessions, with an alpha set at P < .05. All statistical analyses were performed using Statistical Package for the Social Sciences (version 23.0; IBM Corporation, Armonk, NY).

Results

Validity

Third-order polynomials demonstrated the line of best fit between the resting torque outputs at varying intensities of the SIB for both gluteal muscles. The regression analyses with the coefficient of determination (r2) were found to be stronger for the GMax (r2 = .602) than the GMed (r2 = .156) (Figure 3). When evaluating the CAR at varying levels of muscular contractions with the maximal SIB, a linear relationship was the line of best fit for both GMed (r2 = .409) and GMax (r2 = .639) (Figure 4). A significant moderate correlation was identified between hip extension MVIC and CARGMax (r = .51, P = .03); however, no correlation was identified between hip abduction MVIC and CARGMed (r = .19, P = .44).

Figure 3
Figure 3

—Gluteal torque output at graded stimuli at rest.

Citation: Journal of Sport Rehabilitation 29, 7; 10.1123/jsr.2019-0243

Figure 4
Figure 4

—Central activation ratio during progressive maximal voluntary isometric contractions with 100% superimposed burst stimulus.

Citation: Journal of Sport Rehabilitation 29, 7; 10.1123/jsr.2019-0243

Reliability

Between-session reliability of the CARGMed was excellent, ICC(3,k) = .911, and CARGMax was moderately reliable, ICC(3,k) = .704 (Table 2; Supplementary Figures 1 and 2 [available online]). There were no statistical differences observed between the 2 testing sessions for either CARGMed or CARGMax (Table 2). Moderate reliability was observed for both hip abduction MVIC, ICC(3,k) = .606, and SIB, ICC(3,k) = .533, and no differences were detected between hip abduction MVIC and SIB torque (Table 2; Supplementary Figure 1 [available online]). Hip extension MVIC and SIB also had good reliability between testing sessions, ICC(3,k) = .805 and ICC(3,k) = .808, respectively. There were also no differences in hip extension MVIC or SIB (Table 2; Supplementary Figure 2 [available online]).

Table 2

Gluteal Neuromuscular Function Between Day 1 and Day 2

Day 1Day 2ICC(3,k)P value
GMax CAR, %86.50 (7.49)87.20 (10.70).704.74
Hip extension MVIC, N·m/kg2.54 (0.69)2.64 (1.15).805.70
Hip extension SIB, N·m/kg2.88 (0.70)2.91 (1.00).808.90
GMed CAR, %96.10 (3.40)96.60 (3.18).911.60
Hip abduction MVIC, N·m/kg1.56 (0.29)1.57 (0.51).606.88
Hip abduction SIB, N·m/kg1.59 (0.31)1.60 (0.51).533.89

Abbreviations: CAR, central activation ratio; GMax, gluteus maximus; GMed, gluteus medius; ICC, intraclass correlation coefficient; MVIC, maximal voluntary isometric contraction; SIB, superimposed burst.

Discomfort Levels

There was a decrease in VAS scores for both the GMed (day 1: 3.8 [2.4]; day 2: 2.6 [1.6], P = .002) and GMax (day 1: 4.5 [2.3]; day 2: 2.9 [2.1], P < .001) with a lower pain score on the second testing session for both muscles.

Discussion

The purpose of this study was to determine if SIBT was a valid and reliable measure for gluteal activation in healthy individuals. We found that the SIBT was a more valid measurement when assessing the GMax muscle compared with the GMed. In addition, we found a linear relationship between progressive muscular contractions with maximal SIB on gluteal CAR measures. The CAR is a reliable measure for both the GMed and GMax between the 2 testing sessions. We also found patient discomfort during GMed and GMax testing to be comparable with patient discomfort during quadriceps CAR assessments.

Validity

When calculating the CAR, 2 assumptions are required: the participant must provide a maximal contraction and the SIB delivered must be able to recruit all available motor units.14 Therefore, it is essential that the SIB stimulates the maximal number of motor units in the muscle of interest to minimize the potential for underestimating the true activation ratio. To investigate this, we tested progressive stimuli at rest and found a third-order polynomial relationship as the best line of fit for the torque output for both GMed and GMax. This polynomial presents with plateaus at both the lower (25%–50%) and upper (75%–100%) regions of the torque–stimulus curve and a greatest slope between 50% and 75% of the SIB stimulus. With the plateau found in both muscles comparing the 75% and 100% SIB suggests that the electrical stimulus is successfully activating most of the available motor units in the glutes at rest. Interestingly, we did see that the SIB stimulus during rest only accounted for 60.2% of the total variance in hip-extension torque output and 15.6% of the variance in hip abduction in healthy individuals. This may suggest that we were able to get closer to full activation of the GMax, but less with the GMed during rest. The lower accounted variance in the GMed may be due the size of the muscle and the 3 distinct muscle fibers as well as their contributions to not only hip abduction, but also internal and external rotations. However, comparisons between torque output during rest and progressive contractions are limited, and a direct relationship is not known. Future research should evaluate if subtle changes in the stimulus parameters, testing positions, or adipose tissue can influence the percentage of variance accounted for in this measure.

Stackhouse et al23 have evaluated relationships between progressive muscular contractions and the CAR measurement. We found a linear relationship for the CAR of both the GMed and GMax when progressing the percentage of muscular contraction, however, could only explain 40.9% and 63.9% of the variance, respectively. These values are significantly lower compared with the quadriceps muscles, which have been reported above 94% of the variance explained, depending on position and stimulus administered.23 The greater variance explained in the quadriceps could be due to electrodes being positioned over the single muscle group responsible for knee extension, whereas multiple muscles contribute to both hip abduction (GMed, GMax, gluteus minimus, tensor fascia latae, etc) and hip extension (GMax, hamstrings, adductor magnus), and only a single muscle was stimulated in this study. Linear relationships have been found when assessing quadriceps neuromuscular function with the interpolated twitch technique with progressive knee extension contractions.26 However, this technique requires a direct stimulus to the femoral nerve to calculate, and would be challenging to use this technique for the gluteal muscles as the GMax muscle lays directly over the superior and inferior gluteal nerves. Stimulating the nerve directly is likely insufficient at recruiting all motor units of a specific muscle, which may also suggest that the linear relationship observed within our data may not recruit all gluteal motor units. Another interpretation of the linear relationship with the SIBT could be complete activation of the motor units, and the mean CAR values reflect true activation of the gluteal muscles. However, this may be less likely, as the muscles tested have multiple orientations in muscle fibers that contribute to secondary hip motion. There are also additional muscles in the lower-extremity that contribute to both hip abduction and hip extension, which may account for the decrease in both variance during rest and progressive contraction trials when compared with quadriceps data.23

Our findings do differ from previous literature when compared directly to the SIBT, as a curvilinear relationship is more common for quadriceps CAR at varying percentages of maximal effort during knee extension.23 Stackhouse et al23 have found that 75% of voluntary isometric contraction does not produce a change to quadriceps CAR, as the line of best fit being a second-order polynomial. Although we did not see a plateau between the 75% and 100% contractions, these previous studies compared a variety of stimulating frequencies (50–100 Hz) and train duration (120–500 ms). It is possible that the testing and electrode position may play a role, as patient position during knee extension is more isolated during SIBT testing, and the electrodes are directly over the majority of the knee-extensor muscles. Future studies should evaluate how these changes in either the stimulating frequency or train duration would influence the CAR of the gluteal muscles. Stimulus parameters that would optimize both the recruitment of all motor units and achieve maximal discharge rates would be the most accurate at assessing gluteal CAR.23

Muscle strength assessed by the MVIC and CAR provides 2 different methods to assess muscle function. We did identify a moderate relationship between hip extension strength and CARGMax, identifying the 2 measurements have some association in GMax function. However, it is not a perfect linear relationship, suggesting that increases in hip extension strength would not necessarily result in a greater CARGMax. When evaluating GMed hip function, there was no significant correlation between hip abduction MVIC and CARGMed. These 2 measures appear to provide different information about GMed muscle function within a healthy population, and both may be needed to gain a more complete picture of muscle function.

Although we did detect some differences in the GMed variance between the rest and progressive contraction trials, we observed an average CAR of 96.1 and 96.6 between the 2 testing sessions. These values are consistent with previously reported quadriceps CAR values in healthy individuals.14 A CAR below 95 has also been suggested to be threshold for activation failure in the quadriceps muscle.23 We did see a lower CAR value in the GMax, as the group means of the 2 days were 86.5 and 87.2. Although the GMax values are below the 95 threshold commonly seen in the quadriceps, this is the first study to help identify normative values of gluteal muscle activation in a healthy population. It may be plausible that variability in CAR across multiple lower-extremity muscles may exist. Testing position may have an influence on the gluteal CAR values; future studies should evaluate if altering the testing position alters gluteal CAR output.

Reliability

SIBT is a common measurement of neuromuscular function for the quadriceps muscle in healthy individuals27 and pathological groups, such as individuals with patellofemoral pain17 and anterior cruciate ligament–reconstructed populations.15 Reliability of the CAR, MVIC, and SIB has been evaluated on the quadriceps, with limited studies in both healthy and pathological groups. Park and Hopkins16 have found excellent reliability in both the quadriceps MVIC and CAR measures in both within sessions (MVIC: ICC = .99; CAR: ICC = .94) and between sessions (MVIC: ICC = .92; CAR: ICC = .86). The within-session and between-session reliability of the CAR, MVIC, and SIB was also evaluated in individuals with patellofemoral pain.17 The CAR demonstrated fair reliability (ICC = .78), whereas high reliability was found in MVIC (ICC = .96) and SIB (ICC = .96) when assessed 1 week apart.16 Our gluteal MVIC, SIB, and CAR reliability values fall within the range of the previously published literature on the quadriceps.

We did see a greater CAR reliability in our GMed muscle compared with the GMax muscle. This may be due to a variety of factors, such as testing position, electrode placement, and compensation strategies of other muscles to accomplish a task. The GMed muscle is relatively small, and the electrodes used to deliver the stimulus covered a great proportion of the muscle that of the GMax muscle. It is also unknown if compensation strategies exist for the gluteal muscles, as differences in accessory muscle activation have been found during testing of the quadriceps during this assessment.27

Patient Discomfort

One of the limitations with assessing CAR with the SIBT is patient discomfort, due to the stimulus targeting the free nerve endings. We found moderate levels of patient discomfort during both testing sessions for the GMed (VAS = 4.5 and 2.9, respectively) and GMax (3.8 and 2.6, respectively). These values are similar to previous studies that have assessed VAS during quadriceps testing, ranging from 2.2 to 5.3.28 Interestingly, we found lower VAS scores on the second day of testing, which may be due to the longer initial testing session or novelty of the tasks for the participants. These findings may suggest that a familiarization session may be required when assessing gluteal CAR, which is supported in previous findings.17

Limitations

The GMax muscle does present with a challenge in conducting a measure like CAR when assessed by the SIB, as the muscle is triplanar. Attention should be placed on this factor, as the patient positioning for GMax and the location of the electrodes on this muscle may influence torque output and the motor units stimulated. The GMax is responsible for hip rotation, extension, and abduction, so finding a pad placement to optimize our muscle activation could be a potential source of measurement error. Selkowitz et al29 has stated that the superior portion of the GMax produces greater electromyography amplitude than the inferior portion during exercises that incorporated hip abduction and external rotation. Exercises that focused purely on hip extension targeted both portions of the GMax. Another study4 confirmed this theory, stating that hip abduction is greater achieved by the superior GMax due to its insertion on the tensor fascia lata, whereas hip extension is completed by the inferior fibers due a larger moment arm. The mean CAR and ICC values for the GMax were lower than those of the GMed, suggesting that future research should be done to optimize the reliability of GMax strength assessment when attempting to target the fibers responsible for hip extension. Determining optimal patient position and electrode placement on the GMax may also improve the accuracy of assessing CAR of this muscle. Administering a stimulus to the superior portion of the GMax may result in a decrease in hip extension force output due to their more selected role in generating rotational forces for the hip. If a stimulus to the superior fibers resulted in a submaximal hip extension force production, there is a chance that the CAR measure is underestimated and could explain why we had lower reliability values compared with the GMed. In addition, validation of this measure in both larger populations, but also subgroups such as age, sex, and lower-extremity pathology is required. These future studies should also evaluate the magnitude of coefficient of determination of this measure on complete neuromuscular function and determine if optimal methods can improve the variance explained during SIBT testing.

Although finding optimal pad placement is vital in optimizing muscle activation, patient positioning during their MVIC trials may also play a role in correctly assessing muscle activation. A limitation to the current study might have been our patient position during muscle strength testing for the GMed and GMax. Previous studies1,30 have looked at assessing hip abduction in a side-lying position compared with a standing position. We chose to have our patient standing in an effort to minimize the influence of gravity on the participant’s ability to provide maximal effort. Future research should evaluate if the SIBT is reliable at assessing gluteal muscle activation in a variety of testing positions. In addition, evaluating the potential of central activation failure of the gluteal muscles in lower-extremity pathological groups could have large clinically relevant findings. Altered gluteal function has been linked to poor neuromuscular control during functional tasks, so this relationship would also warrants investigation.

Conclusion

The SIBT is a valid and reliable measurement to assess GMed and GMax neuromuscular function in healthy, active individuals. It appears that using similar parameters for assessing the quadriceps is appropriate for measuring gluteal muscle inhibition in a healthy population. Providing patient practice trials and improving participants’ expectations with the SIBT should be considered when using these measures to decrease discomfort during testing. Further investigations using this technique in pathological cohorts must be made before extrapolating this data into clinical practice.

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    Park J, Hopkins JT. Quadriceps activation normative values and the affect of subcutaneous tissue thickness. J Electromyogr Kinesiol. 2011;21(1):136140. PubMed ID: 20947373 doi:10.1016/j.jelekin.2010.09.007

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15.

    Hart JM, Pietrosimone B, Hertel J, Ingersoll CD. Quadriceps activation following knee injuries: a systematic review. J Athl Train. 2010;45(1):8797. PubMed ID: 20064053 doi:10.4085/1062-6050-45.1.87

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16.

    Park J, Hopkins JT. Within- and between-session reliability of the maximal voluntary knee extension torque and activation. Int J Neurosci. 2013;123(1):5559. doi:10.3109/00207454.2012.725117

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17.

    Norte GE, Frye JL, Hart JM. Reliability of the superimposed-burst technique in patients with patellofemoral pain: a technical report. J Athl Train. 2015;50(11):12071211. PubMed ID: 26636730 doi:10.4085/1062-6050-50.10.03

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 18.

    Palmieri RM, Ingersoll CD, Hoffman MA, et al. Arthrogenic muscle response to a simulated ankle joint effusion. Br J Sports Med. 2004;38(1):2630. PubMed ID: 14751941 doi:10.1136/bjsm.2002.001677

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19.

    Drechsler WI, Cramp MC, Scott OM. Changes in muscle strength and EMG median frequency after anterior cruciate ligament reconstruction. Eur J Appl Physiol. 2006;98(6):613623. PubMed ID: 17036217 doi:10.1007/s00421-006-0311-9

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20.

    Hart JM, Fritz JM, Kerrigan DC, Saliba EN, Gansneder BM, Ingersoll CD. Reduced quadriceps activation after lumbar paraspinal fatiguing exercise. J Athl Train. 2006;41(1):7986. PubMed ID: 16619099

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21.

    Pietrosimone BG, Selkow NM, Ingersoll CD, Hart JM, Saliba SA. Electrode type and placement configuration for quadriceps activation evaluation. J Athl Train. 2011;46(6):621628. PubMed ID: 22488187 doi:10.4085/1062-6050-46.6.621

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22.

    Bijur PE, Silver W, Gallagher EJ. Reliability of the visual analog scale for measurement of acute pain. Acad Emerg Med. 2001;8(12):11531157. PubMed ID: 11733293 doi:10.1111/j.1553-2712.2001.tb01132.x

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23.

    Stackhouse SK, Dean JC, Lee SC, Binder-MacLeod SA. Measurement of central activation failure of the quadriceps femoris in healthy adults. Muscle Nerve. 2000;23(11):17061712. PubMed ID: 11054749 doi:10.1002/1097-4598(200011)23:11%3C1706::AID-MUS6%3E3.0.CO;2-B

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24.

    Goetschius J, Hart JM. Knee-extension torque variability and subjective knee function in patients with a history of anterior cruciate ligament reconstruction. J Athl Train. 2016;51(1):2227. doi:10.4085/1062-6050-51.1.12

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25.

    Koo TK, Li MY. A guideline of selecting and reporting intraclass correlation coefficients for reliability research. J Chiropr Med. 2016;15(2):155163. PubMed ID: 27330520 doi:10.1016/j.jcm.2016.02.012

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26.

    Behm D, Power K, Drinkwater E. Comparison of interpolation and central activation ratios as measures of muscle inactivation. Muscle Nerve. 2001;24(7):925934. PubMed ID: 11410920 doi:10.1002/mus.1090

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27.

    Roberts D, Kuenze C, Saliba S, Hart JM. Accessory muscle activation during the superimposed burst technique. J Electromyogr Kinesiol. 2012;22(4):540545. PubMed ID: 22321959 doi:10.1016/j.jelekin.2012.01.008

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28.

    Grindstaff TL, Threlkeld AJ. Optimal stimulation parameters to detect deficits in quadriceps voluntary activation. J Strength Cond Res. 2014;28(2):381389. PubMed ID: 23669820 doi:10.1519/JSC.0b013e3182986d5f

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29.

    Selkowitz DM, Beneck GJ, Powers CM. Comparison of electromyographic activity of the superior and inferior portions of the gluteus maximus muscle during common therapeutic exercises. J Orthop Sports Phys Ther. 2016;46(9):794799. PubMed ID: 27494053 doi:10.2519/jospt.2016.6493

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30.

    Nakagawa TH, Muniz TB, Baldon RM, Maciel CD, Amorim CF, Serrao FV. Electromyographic preactivation pattern of the gluteus medius during weight-bearing functional tasks in women with and without anterior knee pain. Braz J Phys Ther. 2011;15(1):5965. doi:10.1590/S1413-35552011005000003

    • Crossref
    • Search Google Scholar
    • Export Citation

If the inline PDF is not rendering correctly, you can download the PDF file here.

The authors are with the School of Exercise & Rehabilitation Sciences, The University of Toledo, Toledo, OH, USA.

Glaviano (neal.glaviano@utoledo.edu) is corresponding author.
  • View in gallery

    —Participant setup for gluteus medius testing.

  • View in gallery

    —Participant setup for gluteus maximus testing.

  • View in gallery

    —Gluteal torque output at graded stimuli at rest.

  • View in gallery

    —Central activation ratio during progressive maximal voluntary isometric contractions with 100% superimposed burst stimulus.

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    Ward SH, Blackburn JT, Padua DA, et al. Quadriceps neuromuscular function and jump-landing sagittal-plane knee biomechanics after anterior cruciate ligament reconstruction. J Athl Train. 2018;53(2):135143. PubMed ID: 29350554 doi:10.4085/1062-6050-306-16

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    Mizner RL, Stevens JE, Snyder-Mackler L. Voluntary activation and decreased force production of the quadriceps femoris muscle after total knee arthroplasty. Phys Ther. 2003;83(4):359365. PubMed ID: 12665406

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  • 14.

    Park J, Hopkins JT. Quadriceps activation normative values and the affect of subcutaneous tissue thickness. J Electromyogr Kinesiol. 2011;21(1):136140. PubMed ID: 20947373 doi:10.1016/j.jelekin.2010.09.007

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15.

    Hart JM, Pietrosimone B, Hertel J, Ingersoll CD. Quadriceps activation following knee injuries: a systematic review. J Athl Train. 2010;45(1):8797. PubMed ID: 20064053 doi:10.4085/1062-6050-45.1.87

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16.

    Park J, Hopkins JT. Within- and between-session reliability of the maximal voluntary knee extension torque and activation. Int J Neurosci. 2013;123(1):5559. doi:10.3109/00207454.2012.725117

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17.

    Norte GE, Frye JL, Hart JM. Reliability of the superimposed-burst technique in patients with patellofemoral pain: a technical report. J Athl Train. 2015;50(11):12071211. PubMed ID: 26636730 doi:10.4085/1062-6050-50.10.03

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 18.

    Palmieri RM, Ingersoll CD, Hoffman MA, et al. Arthrogenic muscle response to a simulated ankle joint effusion. Br J Sports Med. 2004;38(1):2630. PubMed ID: 14751941 doi:10.1136/bjsm.2002.001677

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19.

    Drechsler WI, Cramp MC, Scott OM. Changes in muscle strength and EMG median frequency after anterior cruciate ligament reconstruction. Eur J Appl Physiol. 2006;98(6):613623. PubMed ID: 17036217 doi:10.1007/s00421-006-0311-9

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20.

    Hart JM, Fritz JM, Kerrigan DC, Saliba EN, Gansneder BM, Ingersoll CD. Reduced quadriceps activation after lumbar paraspinal fatiguing exercise. J Athl Train. 2006;41(1):7986. PubMed ID: 16619099

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21.

    Pietrosimone BG, Selkow NM, Ingersoll CD, Hart JM, Saliba SA. Electrode type and placement configuration for quadriceps activation evaluation. J Athl Train. 2011;46(6):621628. PubMed ID: 22488187 doi:10.4085/1062-6050-46.6.621

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22.

    Bijur PE, Silver W, Gallagher EJ. Reliability of the visual analog scale for measurement of acute pain. Acad Emerg Med. 2001;8(12):11531157. PubMed ID: 11733293 doi:10.1111/j.1553-2712.2001.tb01132.x

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23.

    Stackhouse SK, Dean JC, Lee SC, Binder-MacLeod SA. Measurement of central activation failure of the quadriceps femoris in healthy adults. Muscle Nerve. 2000;23(11):17061712. PubMed ID: 11054749 doi:10.1002/1097-4598(200011)23:11%3C1706::AID-MUS6%3E3.0.CO;2-B

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24.

    Goetschius J, Hart JM. Knee-extension torque variability and subjective knee function in patients with a history of anterior cruciate ligament reconstruction. J Athl Train. 2016;51(1):2227. doi:10.4085/1062-6050-51.1.12

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25.

    Koo TK, Li MY. A guideline of selecting and reporting intraclass correlation coefficients for reliability research. J Chiropr Med. 2016;15(2):155163. PubMed ID: 27330520 doi:10.1016/j.jcm.2016.02.012

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26.

    Behm D, Power K, Drinkwater E. Comparison of interpolation and central activation ratios as measures of muscle inactivation. Muscle Nerve. 2001;24(7):925934. PubMed ID: 11410920 doi:10.1002/mus.1090

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27.

    Roberts D, Kuenze C, Saliba S, Hart JM. Accessory muscle activation during the superimposed burst technique. J Electromyogr Kinesiol. 2012;22(4):540545. PubMed ID: 22321959 doi:10.1016/j.jelekin.2012.01.008

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28.

    Grindstaff TL, Threlkeld AJ. Optimal stimulation parameters to detect deficits in quadriceps voluntary activation. J Strength Cond Res. 2014;28(2):381389. PubMed ID: 23669820 doi:10.1519/JSC.0b013e3182986d5f

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29.

    Selkowitz DM, Beneck GJ, Powers CM. Comparison of electromyographic activity of the superior and inferior portions of the gluteus maximus muscle during common therapeutic exercises. J Orthop Sports Phys Ther. 2016;46(9):794799. PubMed ID: 27494053 doi:10.2519/jospt.2016.6493

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30.

    Nakagawa TH, Muniz TB, Baldon RM, Maciel CD, Amorim CF, Serrao FV. Electromyographic preactivation pattern of the gluteus medius during weight-bearing functional tasks in women with and without anterior knee pain. Braz J Phys Ther. 2011;15(1):5965. doi:10.1590/S1413-35552011005000003

    • Crossref
    • Search Google Scholar
    • Export Citation
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