Manual Therapy xxx (2015) 1e8

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Original article

Differentiation of gluteus medius and minimus activity in weight bearing and non-weight bearing exercises by M-mode ultrasound imaging A. Dieterich a, *, F. Petzke a, C. Pickard b, P. Davey b, D. Falla a, c €ttingen, Go €ttingen, Germany Pain Clinic, Center for Anesthesiology, Emergency and Intensive Care Medicine, University Hospital Go School of Physiotherapy and Exercise Science, Faculty of Health Sciences, Curtin University, Perth, Australia c €ttingen, Germany Department of Neurorehabilitation Engineering, Bernstein Center for Computational Neuroscience, Go a

b

a r t i c l e i n f o

a b s t r a c t

Article history: Received 26 August 2014 Received in revised form 11 January 2015 Accepted 15 January 2015

Background: Knowledge on task-specific activity of the deep hip abductor muscles is limited and is required for determining appropriate hip abductor exercises. Objectives: To assess the temporal differentiation of activity of gluteus minimus and the deep and the superficial 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 minimus and medius muscles in 20 healthy volunteers during weight shift, hip hitch, side-lying abduction and active leg lengthening exercises. M-mode traces were computer-processed for detecting muscle motion onsets. Mean onset differences between muscle regions and their intra-individual variability were assessed. Results: In contrast to side-lying abduction, the weight shift and hip hitch exercises resulted in larger onset variability between the gluteus minimus and deep gluteus medius (P < 0.001) and also between the deep and superficial regions of the gluteus medius (P < 0.05). Conclusions: Weight bearing exercises promoted a greater functional differentiation between deep and superficial hip abductor muscles. © 2015 Elsevier Ltd. All rights reserved.

Keywords: Hip Ultrasound Variability Therapeutic exercise

1. Introduction Deciding whether to use non-weight-bearing or weight-bearing hip abductor exercises in physiotherapy management of hip or knee pathologies includes considerations of the patient's abilities, joint loading, task-specific activation patterns and expected functional gain. However, knowledge of task-specific hip abductor activation patterns is limited, e.g. often evaluation of abductor exercises consider the middle part of the gluteus medius muscle as representative for the hip abductor group. The hip abductor complex comprises, at the deepest level, the gluteus minimus muscle; at the intermediate level, the gluteus medius and piriformis muscles; and at the superficial level, the

€ ttingen, Germany. * Corresponding author. Von-Siebold-Str. 3, D e 37075 Go Tel.: þ49 (0) 551 39 20408. E-mail address: [email protected] (A. Dieterich).

upper portion of the gluteus maximus and the tensor fasciae lata muscles (Grimaldi, 2011). Gluteus medius is further divided into a superficial, medial part and an anterior and a posterior deep part (Jaegers et al., 1992; Grimaldi, 2011). Investigations of hip abductor exercises indicated a task-specific differentiation of gluteus medius relative to tensor fasciae lata and gluteus maximus activity (Boren, 2011; Selkowitz et al., 2013), and also a differential recruitment between parts of the gluteus medius (O'Sullivan et al., 2010). However, exercise studies have been limited to the superficial muscles. Of all hip abductors, gluteus minimus contains the highest percentage of slow twitch fibers (Hitomi et al., 2005) and muscle spindles (Stillman, 2000), rendering the muscle most appropriate for finely adjusted, low force, long-lasting activities. Differential activation has been observed between gluteus minimus and gluteus medius (Wilson et al., 1976; Kumagai et al., 1997) and between the superficial and deep regions of the gluteus medius muscle (Kumagai et al., 1997) suggesting that task-specific muscle

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Please cite this article in press as: Dieterich A, et al., Differentiation of gluteus medius and minimus activity in weight bearing and non-weight bearing exercises by M-mode ultrasound imaging, Manual Therapy (2015), http://dx.doi.org/10.1016/j.math.2015.01.006

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A. Dieterich et al. / Manual Therapy xxx (2015) 1e8

activity does not only include differentiation between adjacent abductor muscles but also between deep and superficial muscles and muscle regions. Located closer to the center of rotation of the hip joint than gluteus medius, gluteus minimus has a shorter lever to produce abduction torque (Neumann, 2010). Considering this biomechanical disadvantage for limb abduction together with the composition of the gluteus minimus muscle, it is suggested that gluteus minimus' specific function is to pull, adjust and hold the acetabulum over the femoral head. Pulling the acetabulum over the femoral head can be addressed in pelvic abduction exercises. In weight bearing, pelvic abduction is facilitated in a ‘pelvic hitch’ exercise, in non-weight bearing by pushing the extended leg in a neutral position in a longitudinal direction (‘active leg lengthening’). It is probable 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 of muscle activity, is invasive, and measures only a small region of a muscle. Magnetic resonance imaging infers activation levels from metabolic changes with limited comparability between subjects (Pattyn et al., 2014) and low temporal resolution. Ultrasound imaging reflects mechanical aspects of muscle activity, typically changes of muscle thickness. M(otion)-mode ultrasound imaging has been used to estimate the onset of deep trunk muscle activity (Vasseljen et al., 2006, 2009) and hip abductor activity (Dieterich et al., 2014) and has been used to demonstrate altered timing of gluteus minimus activity-related muscle motion in subjects with hip pain (Dieterich et al., 2012). M-mode ultrasound enables the measurement of temporal parameters, e.g. onset of activity-related muscle motion in deep and superficial hip abductor muscles. In this study we applied M-mode ultrasound to evaluate the onset of gluteus minimus and gluteus medius (deep and superficial regions) activity-related muscle motion during a selection of hip exercises. We hypothesized that (1) in contrast to abduction in sidelying, exercises in weight bearing would result in differential activation of the gluteus minimus and gluteus medius, indicated by larger onset differences and higher intra-individual variability of the onsets of activity-related muscle motion; (2) a task-dependent differentiation would be observed between deep and superficial regions of the gluteus medius and (3) that subtle, active lengthening of the thigh would facilitate a differentiation between gluteus minimus 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) were recruited via local advertisements. Designed to serve as control subjects in a further study, the participants of the current study were chosen to match a sample of individuals with hip osteoarthritis and represent activation patterns typical for this clinically relevant age group. Inclusion criteria were general good health, absence of hip or lower limb symptoms and age between 40 and 65 years. Exclusion criteria were previous hip surgery, diseases that would affect exercise performance, recurrent pain in the lower limbs or spine, medication potentially affecting reaction time and BMI>32 kg/m2. Participants were physically screened for hip range of motion, manual force testing, and selected hip tests (Faber and Scour test (Cibulka et al., 2009)) which may indicate pathology. Ethical approval for the study was granted by the institutional ethics committee (No. 2/1/13). All procedures were conducted according to the Declaration of Helsinki.

2.2. Procedure Subjects performed in standing (a) weight shift from two-legged to one-legged stance and (b) pelvic abduction (“hip hitch”); in sidelying on a plinth, subjects performed (c) hip abduction and (d) active lengthening of the thigh (Table 1). Each exercise was demonstrated by the investigator and practiced by the participant prior to recording until a correct movement performance was achieved, as evaluated by the investigator. Obvious movement deviations, e.g. into hip flexion or lateral flexion of the trunk were corrected. Individual performance strategies within a correct movement pattern were not influenced. The sequence of the exercises but not of single trials was randomized. Exercises were performed in ten consecutive repetitions with breaks of 10 s or longer between repetitions as required by the participants. Each trial 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 mm footprint (HL9.0/4) set to 6e7 MHz on a mid-section of the hip abductors. A line was drawn connecting the mid-tip of the greater trochanter vertically with the iliac crest. With sufficient gel applied, the transducer was positioned on the line ~1 cm cranial to the greater trochanter. The transducer was housed in a foam block which had been prepared to hold the transducer tilted 20 towards posterior (Ophir et al., 1999); medium density foam allowed for individual angle adjustment. The foam block was fixed around the pelvis with a belt. The gluteus minimus and medius muscles were firstly identified in B-mode ultrasound and the scanning angle adjusted to delineate thin, clear fasciae and intramuscular connective tissue (Fig. 1). To record muscle motion during exercise performance, the ultrasound system was set to M-mode at the highest sweep speed, 2.44 s, providing a temporal resolution of 2.2 ms per pixel. 2.4. Data processing M-mode ultrasound traces were labeled and saved in DICOM format. Traces of the first trial of each exercise, of trials including more than slight baseline motion or a baseline shorter than 400 ms were discarded. From the remaining traces, five to six per exercise and subject were taken randomly for further data analysis. Three levels of analysis were determined, a deep level of 1 cm width within the gluteus minimus, an intermediate level of 1 cm depth within the deeper muscle bulk of the gluteus medius and an upper level of 0.7 cm width adjacent to the superficial fascia of gluteus medius (Fig. 1). The smaller width of the upper level was chosen because no clear visual boundary between differentially moving gluteus medius levels could be identified and the width of the upper level appeared to vary between subjects. Depending on the total image depth, a level of analysis included 59 to 78 pixel lines for the deeper levels and 40 to 50 pixel lines for the upper level. Using a custom programmed LabVIEW application (2013 SP1., National Instruments, Texas, USA), ultrasound grayscale signals of each pixel-line in the depth of analysis were transformed for detecting the signal's energy level by use of the Teager Kaiser Energy 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 the amplitude and frequency of continuous signals (Kaiser, 1990) and has been used on acoustic and EMG signals (Lauer and Prosser, 2009; Solnik et al., 2010; Henriquez Rodriguez et al., 2013). As motion changes the grayscale frequency in M-mode traces, the

Please cite this article in press as: Dieterich A, et al., Differentiation of gluteus medius and minimus activity in weight bearing and non-weight bearing exercises by M-mode ultrasound imaging, Manual Therapy (2015), http://dx.doi.org/10.1016/j.math.2015.01.006

A. Dieterich et al. / Manual Therapy xxx (2015) 1e8

TKEO allows for computed detection of motion onsets (Dieterich et al., 2014). Fully computed onset detection on trials with sufficient baseline quality (see data inclusion) was chosen to ascertain onset reliability. Onset of activity-related muscle motion was defined when the amplitude of the mean rectified TKEOtransformed signals exceeded a threshold of mean baseline amplitude plus four standard deviations for at least 5 of 10 consecutive samples (¼pixels). Computed onset detection is typically relative to a baseline signal (Hodges and Bang, 1996), but ultrasound echoes from far

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(¼deep) contain more noise than echoes from close to the surface. This is comparable to photography; an object in far distance is less sharp than an object nearby. Increased noise leads to increased baseline values, higher onset detection thresholds and less sensitive or later motion detection in deep compared to superficial muscles. Therefore, the comparability of baseline-dependent motion onsets from different depths is uncertain. In order to compare motion onsets of similar intensity between deep and superficial muscles, the onset threshold of gluteus minimus was also applied to the deep gluteus medius. Likewise, the baseline-dependent

Table 1 Hip exercises and their instructions. Exercise

Instruction Start: bilateral quiet stance; “Shift your weight towards your leg with the ultrasound for 1 s and lift the other leg off the floor.”

Start: stance on the leg with ultrasound, the other leg with the forefoot in contact to the floor (a dowel opposite to the stance leg supported quiet standing); “Move your pelvis and hip upwards on the side without the ultrasound”.

(continued on next page)

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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 nobody would notice. Stay on the pillow.”

onset threshold of the deep gluteus medius was used for detecting the onset of the superficial gluteus medius. The main outcome variables were the difference between gluteus minimus and deep gluteus medius onset and the difference between deep and superficial gluteus medius onset. From the exercise repetitions of each subject, mean individual onset differences and their standard deviation were calculated (per exercise). The standard deviation of individual onset differences was processed to assess the variability of the activation pattern (Galna et al., 2013). From all subjects, the median of the onset differences and the median of the standard deviations were determined for each exercise. Large onset differences and high onset variability were considered as indicators of differential activity between muscles/ muscle regions.

3. Results Data from 12 left and 8 right hips were captured. Data inclusion for each exercise is specified in Tables 2 and 3. Missing data, mostly of the leg lengthening exercise, were due to onset detection in less than two trials of an exercise. Participants' hip range of motion was 122 ±10 for flexion, 29 ±5 for abduction and 61 ± 12 for the sum of internal and external rotation. No indications for hip pathology were detected. Fig. 2(aed) provide representative M-mode traces of each exercise for one subject.

2.5. Statistical analysis The distributions of deep (gluteus minimus to deep gluteus medius) and superficial (deep to superficial gluteus medius) onset differences were assessed by boxplots. Accounting for skewness in some distributions, all onset differences were described by median and interquartile range (IQR). Differences between the weight bearing exercises and side-lying abduction exercise were examined using one-way repeated measures ANOVA. If Mauchly's test of sphericity was significant, meaning that the assumption of similar variances was violated, Greenhouse-Geisser correction of the degrees of freedom was applied. Post-hoc comparisons with NewmaneKeuls test were used to specify significantly different exercise(s) (Field, 2009). The same statistical analyses, boxplots and one-way repeated measures ANOVA, were applied to examine differences in intraindividual onset variability between exercises. Statistical analysis was 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.

Fig. 1. B-mode ultrasound image of gluteus minimus (Gmin) and gluteus medius (Gmed). The white vertical lines mark the regions of analysis.

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Table 2 Median and interquartile range (IQR) of mean onset differences and intra-individual standard deviation of onset differences between gluteus minimus and the deep gluteus medius per exercise (incl. outliers).

Onset difference, median (IQR), s SD of individual onset differences, median (IQR), s

Weight shift (n 19)

Hip hitch (n 17)

Abduction in side-lying (n 20)

Leg lengthening (n 12)

0.056 (0.129) 0.095 (0.104)

0.002 (0.051) 0.026 (0.101)

0.010 (0.017) 0.010 (0.012)

0.009 (0.034) 0.022 (0.043)

Table 3 Median and interquartile range (IQR) of mean onset differences and intra-individual standard deviation of onset differences between the deep and superficial regions of gluteus medius per exercise (incl. outliers).

Onset difference, median (IQR), s SD individual onset differences, median (IQR), s

Weight shift (n 20)

Hip hitch (n 19)

Abduction in side-lying (n 19)

Leg lengthening (n 11)

0.072 (0.128) 0.081 (0.077)

0.029 (0.038) 0.021 (0.034)

0.018 (0.031) 0.013 (0.044)

0.051 (0.072) 0.026 (0.087)

3.1. Differentiation between the gluteus minimus and the deep gluteus medius In all exercises the majority of onset differences was positive, meaning that gluteus minimus motion was detected before deep gluteus 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) differed between exercises (F ¼ 10.21; P < 0.001), with significant differences observed between weight shift and side-lying abduction (P < 0.001), hip hitch and side-lying abduction (P ¼ 0.02) and weight shift and hip hitch (P ¼ 0.04). 3.2. Differentiation between the deep and the superficial regions of gluteus medius In all exercises, the majority of onset differences were positive, meaning that deep gluteus medius motion was detected before

superficial gluteus medius motion (Fig. 4). Mean onset differences (Table 3) were significantly different between exercises, with Greenhouse-Geisser correction (F ¼ 4.24; P ¼ 0.04). Post-hoc comparisons with NewmaneKeuls test indicated a significant difference between weight shift and side-lying abduction (P ¼ 0.02). The evaluation of intra-individual variability (Table 3) confirmed differences between exercises (F ¼ 5.33; P ¼ 0.02; with Greenhouse-Geisser correction), with significant differences observed 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 gluteus medius in the ‘active leg lengthening’ exercise Onset differences in the ‘active leg lengthening’ exercise and their variability were not significantly different from side-lying abduction or from the weight bearing exercises. An insignificant trend towards higher onset variation could be noted (Figs. 3 and 4).

Fig. 2. a) weight shift, b) hip hitch, c) side-lying abduction, d) leg lengthening: Representative M-mode traces of the exercises. Note that representativeness of single trials is limited. Main distinguishing features observable in these examples are higher baseline motion and earlier motion onset in gluteus minimus for weight shift, synchronous motion onset for side-lying abduction, predominantly deep muscle motion for active leg lengthening.

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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 boxes represent 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 distance from 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 boxes represent 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 distance from the box) are not shown. Significant differences *P < 0.05.

4. Discussion M-mode ultrasound imaging revealed different patterns of the onset of activity-related hip muscle motion between hip exercises. Compared to hip abduction in side-lying, the weight bearing exercises, ‘weight shift to one-legged stance’ and ‘hip hitch’, showed a higher differentiation between gluteus minimus and deep gluteus medius activity onsets revealed by larger individual variability of onset differences. Larger differentiation of muscle motion onsets in weight bearing exercises were also observable between the deep and the superficial gluteus medius regions. The ‘active leg lengthening exercise’ showed only a non-significant trend towards a higher differentiation of activity of hip abductor muscles and muscle regions. Side-lying abduction featured only minimal onset differences and minimal onset variability between gluteus minimus and the deep gluteus medius muscle. In contrast, for the weight shift

and hip hitch exercises, the time span between gluteus minimus and deep gluteus medius onset was highly variable with onset differences up to 200 ms. The quasi simultaneous motion onset in side-lying abduction suggests a synchronous muscle recruitment; gluteus minimus and the deep gluteus medius contribute to the same function of pulling the thigh into hip abduction. The high variability between gluteus minimus and the deep gluteus medius in weight bearing suggests a functional differentiation, e.g. an adaption to slight differences in the position of the center of mass (Safavynia and Ting, 2012) or other mechanical demands (Herrel et al., 2008). The study findings suggest that such differentiation can be exercised in weight shift to one legged stance but not in side-lying abduction. In agreement with higher functional demands by weight bearing exercises, increased functional gain from weight bearing compared to non-weight bearing hip rehabilitation has been documented (Tsukagoshi et 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 adjusting function of gluteus minimus. A structural need for a differentiated gluteus minimus recruitment in weight bearing may be provided by the physiological incongruence of the hip joint (Menschik, 1997) which provides space for translations of the femoral head (Harding et al., 2003). Finely adjusted muscle activity close to the center of joint rotation may be needed to position the acetabulum optimally on the femoral head for loading, in order to avoid excessive stress (Lewis and Sahrmann, 2006). From this perspective, the smaller variability observed for the hip hitch compared to weight shift exercise would be explainable because the hip hitch exercise started in supported one-legged stance; most adjustments to weighttransfer occurred before the exercise started. The task-dependent differentiation between activity of the deep and the superficial gluteus medius regions was significant but smaller than the difference observed between gluteus minimus and deep gluteus medius (Figs. 3 and 4). The gluteus medius parts can be distinguished by muscle fiber direction (Gottschalk et al., 1989). Fibers are orientated vertical in the ventral and middle muscle parts and horizontal, parallel to the femoral neck in the posterior part (Gottschalk et al., 1989). Therefore, gluteus medius parts address different degrees of femoral internal to external rotation (Neumann, 2010). Gluteus medius parts overlap with the posterior part being deepest (Gottschalk et al., 1989; Al-Hayani, 2009). A differentiation between deep and superficial regions of gluteus medius may be related to adjusting femoral rotation during activity. Why were the mean onset differences not different between exercises? As the boxplots (Figs. 3 and 4, left) demonstrate, onset variability occurred into positive and negative directions, leading to cancellation effects. Technical limitations could also have played a role. The higher noise levels with larger depth may have obscured slight gluteus minimus motion onsets, a possible cause of negative onset differences. Standardizing the analysis to 1 cm of muscle per level for all subjects led to a differing number of pixel lines being analyzed depending on the total muscle depth. Extending the analysis over the full depth of each muscle may have been an advantageous approach. Another potential influence is the different grayscale appearance between muscle levels. The TKEO signal transformation is sensitive to grayscale amplitude, which needs to be similar between depth levels. Suboptimal image settings may have influenced onset detection, in spite of efforts to adjust accordingly. Current interpretations of activity-related motion are limited. EMG and ultrasound measurements of muscle activity are not equivalent (Vasseljen et al., 2006; Dieterich et al., 2014). Differences in sample volume and the influence of mechanical motion transmission contribute to discrepancies between electrical and mechanical aspects of muscle activity. In order to minimize the influence of motion transmission from limb or trunk motion, exercise performance included only little limb or pelvic motion and started from a relaxed or quiet situation. Considering the technical influences, the explorative character of the study must be emphasized. The innovative M-mode method provided non-invasive observations of deep muscle activity which enabled measurements of differences between exercises. Muscle motion patterns can be observed readily in M-mode without computed methods (Fig. 2), providing potential utility for clinical assessments and exercise feedback. 4.1. Conclusion The study findings support a differentiated, task-dependent recruitment within deep and superficial levels of the hip abductor complex. In healthy participants, weight bearing exercises

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Please cite this article in press as: Dieterich A, et al., Differentiation of gluteus medius and minimus activity in weight bearing and non-weight bearing exercises by M-mode ultrasound imaging, Manual Therapy (2015), http://dx.doi.org/10.1016/j.math.2015.01.006

Differentiation of gluteus medius and minimus activity in weight bearing and non-weight bearing exercises by M-mode ultrasound imaging.

Knowledge on task-specific activity of the deep hip abductor muscles is limited and is required for determining appropriate hip abductor exercises...
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