Differentiation of gluteus medius and minimus activity in weightbearing and non-weight bearing exercises by M-mode ultrasoundimaging
A. Dieterich a, *, F. Petzke a, C. Pickard b, P. Davey b, D. Falla a, c
a Pain Clinic, Center for Anesthesiology, Emergency and Intensive Care Medicine, University Hospital G€ottingen, G€ottingen, Germanyb School of Physiotherapy and Exercise Science, Faculty of Health Sciences, Curtin University, Perth, Australiac Department of Neurorehabilitation Engineering, Bernstein Center for Computational Neuroscience, G€ottingen, Germany
a r t i c l e i n f o
Article history:Received 26 August 2014Received in revised form11 January 2015Accepted 15 January 2015
Background: Knowledge on task-specific activity of the deep hip abductor muscles is limited and isrequired for determining appropriate hip abductor exercises.Objectives: To assess the temporal differentiation of activity of gluteus minimus and the deep and thesuperficial regions of gluteus medius during weight bearing and non-weight bearing exercises.Design: Repeated measures design on a single recording occasion.Method: M-mode ultrasound was used to capture activity-related muscle motion of the gluteus minimusand medius muscles in 20 healthy volunteers during weight shift, hip hitch, side-lying abduction andactive leg lengthening exercises. M-mode traces were computer-processed for detecting muscle motiononsets. Mean onset differences between muscle regions and their intra-individual variability wereassessed.Results: In contrast to side-lying abduction, the weight shift and hip hitch exercises resulted in largeronset variability between the gluteus minimus and deep gluteus medius (P < 0.001) and also betweenthe deep and superficial regions of the gluteus medius (P < 0.05).Conclusions: Weight bearing exercises promoted a greater functional differentiation between deep andsuperficial hip abductor muscles.
Deciding whether to use non-weight-bearing or weight-bearinghip abductor exercises in physiotherapy management of hip orknee pathologies includes considerations of the patient's abilities,joint loading, task-specific activation patterns and expected func-tional gain. However, knowledge of task-specific hip abductoractivation patterns is limited, e.g. often evaluation of abductor ex-ercises consider the middle part of the gluteus medius muscle asrepresentative for the hip abductor group.
The hip abductor complex comprises, at the deepest level, thegluteus minimus muscle; at the intermediate level, the gluteusmedius and piriformis muscles; and at the superficial level, the
37075 G€ottingen, Germany.
gen.de (A. Dieterich).
upper portion of the gluteus maximus and the tensor fasciae latamuscles (Grimaldi, 2011). Gluteus medius is further divided into asuperficial, medial part and an anterior and a posterior deep part(Jaegers et al., 1992; Grimaldi, 2011). Investigations of hip abductorexercises indicated a task-specific differentiation of gluteus mediusrelative to tensor fasciae lata and gluteus maximus activity (Boren,2011; Selkowitz et al., 2013), and also a differential recruitmentbetween parts of the gluteus medius (O'Sullivan et al., 2010).However, exercise studies have been limited to the superficialmuscles.
Of all hip abductors, gluteus minimus contains the highestpercentage of slow twitch fibers (Hitomi et al., 2005) and musclespindles (Stillman, 2000), rendering the muscle most appropriatefor finely adjusted, low force, long-lasting activities. Differentialactivation has been observed between gluteus minimus andgluteus medius (Wilson et al., 1976; Kumagai et al., 1997) and be-tween the superficial and deep regions of the gluteus mediusmuscle (Kumagai et al., 1997) suggesting that task-specific muscle
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activity does not only include differentiation between adjacentabductor muscles but also between deep and superficial musclesand muscle regions.
Located closer to the center of rotation of the hip joint thangluteus medius, gluteus minimus has a shorter lever to produceabduction torque (Neumann, 2010). Considering this biomechan-ical disadvantage for limb abduction together with the compositionof the gluteus minimus muscle, it is suggested that gluteus mini-mus' specific function is to pull, adjust and hold the acetabulumover the femoral head. Pulling the acetabulum over the femoralhead can be addressed in pelvic abduction exercises. In weightbearing, pelvic abduction is facilitated in a ‘pelvic hitch’ exercise, innon-weight bearing by pushing the extended leg in a neutral po-sition in a longitudinal direction (‘active leg lengthening’). It isprobable that the lengthening should be performed in a subtle,slow manner to predominantly facilitate gluteus minimus.
Current methods to assess deep hip abductor activity are limited.Fine-wire electromyography (EMG) measures electrical aspects ofmuscle activity, is invasive, and measures only a small region of amuscle. Magnetic resonance imaging infers activation levels frommetabolic changes with limited comparability between subjects(Pattyn et al., 2014) and low temporal resolution. Ultrasound im-aging reflects mechanical aspects of muscle activity, typicallychanges of muscle thickness. M(otion)-mode ultrasound imaginghas been used to estimate the onset of deep trunk muscle activity(Vasseljen et al., 2006, 2009) and hip abductor activity (Dieterichet al., 2014) and has been used to demonstrate altered timing ofgluteus minimus activity-related muscle motion in subjects withhip pain (Dieterich et al., 2012). M-mode ultrasound enables themeasurement of temporal parameters, e.g. onset of activity-relatedmuscle motion in deep and superficial hip abductor muscles.
In this study we applied M-mode ultrasound to evaluate theonset of gluteus minimus and gluteus medius (deep and superficialregions) activity-related muscle motion during a selection of hipexercises.We hypothesized that (1) in contrast to abduction in side-lying, exercises in weight bearing would result in differential acti-vation of the gluteus minimus and gluteus medius, indicated bylarger onset differences and higher intra-individual variability ofthe onsets of activity-related muscle motion; (2) a task-dependentdifferentiation would be observed between deep and superficialregions of the gluteus medius and (3) that subtle, active length-ening of the thighwould facilitate a differentiation between gluteusminimus and gluteus medius in non-weight bearing.
2. Methods
2.1. Participants
Twenty (12 women) healthy volunteers (age; mean ± SD:54.9 ± 7.0 years, range 42e65 years, BMI: 23.7 ± 2.8 kg/m2) wererecruited via local advertisements. Designed to serve as controlsubjects in a further study, the participants of the current studywere chosen to match a sample of individuals with hip osteoar-thritis and represent activation patterns typical for this clinicallyrelevant age group. Inclusion criteria were general good health,absence of hip or lower limb symptoms and age between 40 and 65years. Exclusion criteria were previous hip surgery, diseases thatwould affect exercise performance, recurrent pain in the lowerlimbs or spine, medication potentially affecting reaction time andBMI>32 kg/m2. Participants were physically screened for hip rangeof motion, manual force testing, and selected hip tests (Faber andScour test (Cibulka et al., 2009)) which may indicate pathology.Ethical approval for the study was granted by the institutionalethics committee (No. 2/1/13). All procedures were conducted ac-cording to the Declaration of Helsinki.
2.2. Procedure
Subjects performed in standing (a) weight shift from two-leggedto one-legged stance and (b) pelvic abduction (“hip hitch”); in side-lying on a plinth, subjects performed (c) hip abduction and (d)active lengthening of the thigh (Table 1). Each exercise wasdemonstrated by the investigator and practiced by the participantprior to recording until a correct movement performance wasachieved, as evaluated by the investigator. Obvious movementdeviations, e.g. into hip flexion or lateral flexion of the trunk werecorrected. Individual performance strategies within a correctmovement pattern were not influenced. The sequence of the ex-ercises but not of single trials was randomized. Exercises wereperformed in ten consecutive repetitions with breaks of 10 s orlonger between repetitions as required by the participants. Eachtrial was recorded separately.
2.3. Ultrasound imaging
Ultrasonography was recorded using a Logic Scan 128 system(Telemed Ltd. Vilnius, Lithuania) with a linear transducer of 40 mmfootprint (HL9.0/4) set to 6e7 MHz on a mid-section of the hipabductors. A line was drawn connecting the mid-tip of the greatertrochanter vertically with the iliac crest. With sufficient gel applied,the transducer was positioned on the line ~1 cm cranial to thegreater trochanter. The transducer was housed in a foam blockwhich had been prepared to hold the transducer tilted 20� towardsposterior (Ophir et al., 1999); medium density foam allowed forindividual angle adjustment. The foam block was fixed around thepelvis with a belt. The gluteus minimus and medius muscles werefirstly identified in B-mode ultrasound and the scanning angleadjusted to delineate thin, clear fasciae and intramuscular con-nective tissue (Fig. 1). To record muscle motion during exerciseperformance, the ultrasound system was set to M-mode at thehighest sweep speed, 2.44 s, providing a temporal resolution of2.2 ms per pixel.
2.4. Data processing
M-mode ultrasound traces were labeled and saved in DICOMformat. Traces of the first trial of each exercise, of trials includingmore than slight baseline motion or a baseline shorter than 400 mswere discarded. From the remaining traces, five to six per exerciseand subject were taken randomly for further data analysis.
Three levels of analysis were determined, a deep level of 1 cmwidth within the gluteus minimus, an intermediate level of 1 cmdepth within the deeper muscle bulk of the gluteus medius and anupper level of 0.7 cm width adjacent to the superficial fascia ofgluteus medius (Fig. 1). The smaller width of the upper level waschosen because no clear visual boundary between differentiallymoving gluteus medius levels could be identified and the width ofthe upper level appeared to vary between subjects. Depending onthe total image depth, a level of analysis included 59 to 78 pixellines for the deeper levels and 40 to 50 pixel lines for the upperlevel.
Using a custom programmed LabVIEW application (2013 SP1.,National Instruments, Texas, USA), ultrasound grayscale signals ofeach pixel-line in the depth of analysis were transformed fordetecting the signal's energy level by use of the Teager Kaiser En-ergy Operator (TKEO); TKEO ¼ x2(n) � x(n � 1)*x(n þ 1) (Li et al.,2007; Dieterich et al., 2014). The TKEO indicates changes in theamplitude and frequency of continuous signals (Kaiser, 1990) andhas been used on acoustic and EMG signals (Lauer and Prosser,2009; Solnik et al., 2010; Henriquez Rodriguez et al., 2013). Asmotion changes the grayscale frequency in M-mode traces, the
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TKEO allows for computed detection of motion onsets (Dieterichet al., 2014). Fully computed onset detection on trials with suffi-cient baseline quality (see data inclusion) was chosen to ascertainonset reliability. Onset of activity-related muscle motion wasdefined when the amplitude of the mean rectified TKEO-transformed signals exceeded a threshold of mean baselineamplitude plus four standard deviations for at least 5 of 10consecutive samples (¼pixels).
Computed onset detection is typically relative to a baselinesignal (Hodges and Bang, 1996), but ultrasound echoes from far
Table 1Hip exercises and their instructions.
Exercise Instructi
Start: bil“Shift yofloor.”
Start: stafloor (a d“Move y
(¼deep) contain more noise than echoes from close to the surface.This is comparable to photography; an object in far distance is lesssharp than an object nearby. Increased noise leads to increasedbaseline values, higher onset detection thresholds and less sensi-tive or later motion detection in deep compared to superficialmuscles. Therefore, the comparability of baseline-dependent mo-tion onsets from different depths is uncertain. In order to comparemotion onsets of similar intensity between deep and superficialmuscles, the onset threshold of gluteus minimus was also appliedto the deep gluteus medius. Likewise, the baseline-dependent
on
ateral quiet stance;ur weight towards your leg with the ultrasound for 1 s and lift the other leg off the
nce on the leg with ultrasound, the other leg with the forefoot in contact to theowel opposite to the stance leg supported quiet standing);our pelvis and hip upwards on the side without the ultrasound”.
(continued on next page)
Table 1 (continued )
Exercise Instruction
Start: side-lying, upper leg relaxed on supporting pillow, lower leg flexed;“lift your foot and leg up slightly so that you lose contact to the pillow”.
Start: side-lying, upper leg relaxed on supporting pillow, lower leg flexed;“slowly with subtlety lengthen your thigh as if your leg is growing longer, but nobodywould notice. Stay on the pillow.”
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onset threshold of the deep gluteus medius was used for detectingthe onset of the superficial gluteus medius.
The main outcome variables were the difference betweengluteus minimus and deep gluteus medius onset and the differencebetween deep and superficial gluteus medius onset. From the ex-ercise repetitions of each subject, mean individual onset differencesand their standard deviation were calculated (per exercise). Thestandard deviation of individual onset differences was processed toassess the variability of the activation pattern (Galna et al., 2013).From all subjects, the median of the onset differences and themedian of the standard deviations were determined for each ex-ercise. Large onset differences and high onset variability wereconsidered as indicators of differential activity between muscles/muscle regions.
Fig. 1. B-mode ultrasound image of gluteus minimus (Gmin) and gluteus medius(Gmed). The white vertical lines mark the regions of analysis.
2.5. Statistical analysis
The distributions of deep (gluteus minimus to deep gluteusmedius) and superficial (deep to superficial gluteus medius) onsetdifferences were assessed by boxplots. Accounting for skewness insome distributions, all onset differences were described by medianand interquartile range (IQR). Differences between the weightbearing exercises and side-lying abduction exercise were examinedusing one-way repeated measures ANOVA. If Mauchly's test ofsphericity was significant, meaning that the assumption of similarvariances was violated, Greenhouse-Geisser correction of the de-grees of freedom was applied. Post-hoc comparisons with New-maneKeuls test were used to specify significantly differentexercise(s) (Field, 2009).
The same statistical analyses, boxplots and one-way repeatedmeasures ANOVA, were applied to examine differences in intra-individual onset variability between exercises. Statistical analysiswas performed using SPSS 17 (IBM Corporation, Armonk, New York,USA) and Statistica 7 (StatSoft Inc., Dell Software, Aliso Viejo, CA,USA) with P < 0.05 as level of significance.
3. Results
Data from 12 left and 8 right hips were captured. Data inclusionfor each exercise is specified in Tables 2 and 3. Missing data, mostlyof the leg lengthening exercise, were due to onset detection in lessthan two trials of an exercise. Participants' hip range of motionwas122�±10� for flexion, 29�±5� for abduction and 61�± 12� for thesum of internal and external rotation. No indications for hip pa-thology were detected.
Fig. 2(aed) provide representative M-mode traces of each ex-ercise for one subject.
Table 2Median and interquartile range (IQR) of mean onset differences and intra-individual standard deviation of onset differences between gluteus minimus and the deep gluteusmedius per exercise (incl. outliers).
Weight shift (n 19) Hip hitch (n 17) Abduction in side-lying (n 20) Leg lengthening (n 12)
Onset difference, median (IQR), s 0.056 (0.129) 0.002 (0.051) 0.010 (0.017) 0.009 (0.034)SD of individual onset differences, median (IQR), s 0.095 (0.104) 0.026 (0.101) 0.010 (0.012) 0.022 (0.043)
Table 3Median and interquartile range (IQR) of mean onset differences and intra-individual standard deviation of onset differences between the deep and superficial regions ofgluteus medius per exercise (incl. outliers).
Weight shift (n 20) Hip hitch (n 19) Abduction in side-lying (n 19) Leg lengthening (n 11)
Onset difference, median (IQR), s 0.072 (0.128) 0.029 (0.038) 0.018 (0.031) 0.051 (0.072)SD individual onset differences, median (IQR), s 0.081 (0.077) 0.021 (0.034) 0.013 (0.044) 0.026 (0.087)
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3.1. Differentiation between the gluteus minimus and the deepgluteus medius
In all exercises the majority of onset differences was positive,meaning that gluteus minimus motion was detected before deepgluteus medius motion (Fig. 3). Mean onset differences (Table 2)were not significantly different between exercises (F ¼ 1.20;P ¼ 0.32). However, intra-individual variability (Table 2) differedbetween exercises (F ¼ 10.21; P < 0.001), with significant differ-ences observed between weight shift and side-lying abduction(P < 0.001), hip hitch and side-lying abduction (P ¼ 0.02) andweight shift and hip hitch (P ¼ 0.04).
3.2. Differentiation between the deep and the superficial regions ofgluteus medius
In all exercises, the majority of onset differences were positive,meaning that deep gluteus medius motion was detected before
Fig. 2. a) weight shift, b) hip hitch, c) side-lying abduction, d) leg lengthening: RepresentativMain distinguishing features observable in these examples are higher baseline motion and eside-lying abduction, predominantly deep muscle motion for active leg lengthening.
superficial gluteus medius motion (Fig. 4). Mean onset differences(Table 3) were significantly different between exercises, withGreenhouse-Geisser correction (F ¼ 4.24; P ¼ 0.04). Post-hoccomparisons with NewmaneKeuls test indicated a significant dif-ference between weight shift and side-lying abduction (P ¼ 0.02).The evaluation of intra-individual variability (Table 3) confirmeddifferences between exercises (F ¼ 5.33; P ¼ 0.02; withGreenhouse-Geisser correction), with significant differencesobserved between weight shift and side-lying abduction (P ¼ 0.01)and between weight shift and hip hitch (P ¼ 0.01).
3.3. Differentiation between gluteus minimus and deep gluteusmedius in the ‘active leg lengthening’ exercise
Onset differences in the ‘active leg lengthening’ exercise andtheir variability were not significantly different from side-lyingabduction or from the weight bearing exercises. An insignificanttrend towards higher onset variation could be noted (Figs. 3 and 4).
e M-mode traces of the exercises. Note that representativeness of single trials is limited.arlier motion onset in gluteus minimus for weight shift, synchronous motion onset for
Fig. 3. Mean onset differences (a) and intra-individual standard deviation of onset differences (b) between gluteus minimus and the deep gluteus medius per exercise. The boxesrepresent the interquartile range (IQR) between the 25th to 75th percentiles of onset differences; the horizontal line in the box represents the median. Outliers (>1.5 IQR distancefrom the box) are not shown. Significant differences *P < 0.05, **P < 0.001.
***
Fig. 4. Mean onset differences (a) and intra-individual standard deviation of onset differences (b) between the deep and the superficial gluteus medius per exercise. The boxesrepresent the interquartile range (IQR) between the 25th to 75th percentiles of onset differences; the horizontal line in the box represents the median. Outliers (>1.5 IQR distancefrom the box) are not shown. Significant differences *P < 0.05.
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4. Discussion
M-mode ultrasound imaging revealed different patterns of theonset of activity-related hip muscle motion between hip exercises.Compared to hip abduction in side-lying, the weight bearing ex-ercises, ‘weight shift to one-legged stance’ and ‘hip hitch’, showed ahigher differentiation between gluteus minimus and deep gluteusmedius activity onsets revealed by larger individual variability ofonset differences. Larger differentiation of muscle motion onsets inweight bearing exercises were also observable between the deepand the superficial gluteus medius regions. The ‘active leg length-ening exercise’ showed only a non-significant trend towards ahigher differentiation of activity of hip abductor muscles andmuscle regions.
Side-lying abduction featured only minimal onset differencesand minimal onset variability between gluteus minimus and thedeep gluteus medius muscle. In contrast, for the weight shift
and hip hitch exercises, the time span between gluteus minimusand deep gluteus medius onset was highly variable with onsetdifferences up to 200 ms. The quasi simultaneous motion onsetin side-lying abduction suggests a synchronous muscle recruit-ment; gluteus minimus and the deep gluteus medius contributeto the same function of pulling the thigh into hip abduction. Thehigh variability between gluteus minimus and the deep gluteusmedius in weight bearing suggests a functional differentiation,e.g. an adaption to slight differences in the position of the centerof mass (Safavynia and Ting, 2012) or other mechanical de-mands (Herrel et al., 2008). The study findings suggest that suchdifferentiation can be exercised in weight shift to one leggedstance but not in side-lying abduction. In agreement with higherfunctional demands by weight bearing exercises, increasedfunctional gain from weight bearing compared to non-weightbearing hip rehabilitation has been documented (Tsukagoshiet al., 2014).
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The high content of sensory elements and slow twitch fibers(Stillman, 2000; Hitomi et al., 2005) supports a finely adjustingfunction of gluteus minimus. A structural need for a differentiatedgluteus minimus recruitment in weight bearing may be providedby the physiological incongruence of the hip joint (Menschik, 1997)which provides space for translations of the femoral head (Hardinget al., 2003). Finely adjusted muscle activity close to the center ofjoint rotation may be needed to position the acetabulum optimallyon the femoral head for loading, in order to avoid excessive stress(Lewis and Sahrmann, 2006). From this perspective, the smallervariability observed for the hip hitch compared to weight shiftexercise would be explainable because the hip hitch exercise star-ted in supported one-legged stance; most adjustments to weight-transfer occurred before the exercise started.
The task-dependent differentiation between activity of the deepand the superficial gluteus medius regions was significant butsmaller than the difference observed between gluteusminimus anddeep gluteus medius (Figs. 3 and 4). The gluteus medius parts canbe distinguished by muscle fiber direction (Gottschalk et al., 1989).Fibers are orientated vertical in the ventral and middle muscleparts and horizontal, parallel to the femoral neck in the posteriorpart (Gottschalk et al., 1989). Therefore, gluteus medius partsaddress different degrees of femoral internal to external rotation(Neumann, 2010). Gluteus medius parts overlap with the posteriorpart being deepest (Gottschalk et al., 1989; Al-Hayani, 2009). Adifferentiation between deep and superficial regions of gluteusmediusmay be related to adjusting femoral rotation during activity.
Why were the mean onset differences not different betweenexercises? As the boxplots (Figs. 3 and 4, left) demonstrate, onsetvariability occurred into positive and negative directions, leading tocancellation effects. Technical limitations could also have played arole. The higher noise levels with larger depth may have obscuredslight gluteus minimus motion onsets, a possible cause of negativeonset differences. Standardizing the analysis to 1 cm of muscle perlevel for all subjects led to a differing number of pixel lines beinganalyzed depending on the total muscle depth. Extending theanalysis over the full depth of each muscle may have been an ad-vantageous approach. Another potential influence is the differentgrayscale appearance between muscle levels. The TKEO signaltransformation is sensitive to grayscale amplitude, which needs tobe similar between depth levels. Suboptimal image settings mayhave influenced onset detection, in spite of efforts to adjustaccordingly.
Current interpretations of activity-related motion are limited.EMG and ultrasound measurements of muscle activity are notequivalent (Vasseljen et al., 2006; Dieterich et al., 2014). Differencesin sample volume and the influence of mechanical motion trans-mission contribute to discrepancies between electrical and me-chanical aspects of muscle activity. In order to minimize theinfluence of motion transmission from limb or trunk motion, ex-ercise performance included only little limb or pelvic motion andstarted from a relaxed or quiet situation.
Considering the technical influences, the explorative characterof the study must be emphasized. The innovative M-mode methodprovided non-invasive observations of deep muscle activity whichenabled measurements of differences between exercises. Musclemotion patterns can be observed readily in M-mode withoutcomputed methods (Fig. 2), providing potential utility for clinicalassessments and exercise feedback.
4.1. Conclusion
The study findings support a differentiated, task-dependentrecruitment within deep and superficial levels of the hipabductor complex. In healthy participants, weight bearing exercises
addressed a functional differentiation between gluteus minimusand gluteus medius, which was not observable in side-lyingabduction.
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