Reliability of Abdominal Muscle Stiffness Measured Using Elastography during Trunk Rehabilitation Exercises

Ultrasound in Med. & Biol., Vol. -, No. -, pp. 1–8, 2015 Copyright Ó 2015 World Federation for Ultrasound in Medicine & Biology Printed in the USA. All rights reserved 0301-5629/$ - see front matter

http://dx.doi.org/10.1016/j.ultrasmedbio.2015.12.002

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Technical Note RELIABILITY OF ABDOMINAL MUSCLE STIFFNESS MEASURED USING ELASTOGRAPHY DURING TRUNK REHABILITATION EXERCISES DAVID MACDONALD,* ALAN WAN,* MEGAN MCPHEE,* KYLIE TUCKER,y and FRANC¸ OIS HUG*z * School of Health and Rehabilitation Sciences, University of Queensland, Brisbane, QLD, Australia; y School of Biomedical Sciences, University of Queensland, Brisbane, QLD, Australia; and z Laboratory ‘‘Movement, Interactions, Performance’’ (EA 4334), UFR STAPS, University of Nantes, Nantes, France (Received 12 September 2015; revised 29 October 2015; in final form 7 December 2015)

Abstract—The aim of this study was to assess the intra-session and inter-rater reliability of shear modulus measured in abdominal muscles during two commonly used trunk stability exercises. Thirty healthy volunteers performed a series of abdominal hollow and abdominal brace tasks. Supersonic shear imaging was used to measure the shear modulus (considered an index of muscle tension) of the four anterior trunk muscles: obliquus externus abdominis, obliquus internus abdominis, transversus abdominis and rectus abdominis. Because of measurement artifacts, internus abdominis and transversus abdominis data were not analyzed for 36.7% and 26.7% of the participants, respectively. These participants exhibited thicker superficial fat layers than the others. For the remaining participants, fair to excellent intra-session and inter-rater reliability was observed with moderate to high intraclass coefficients (0.45–0.97) and low to moderate standard error of measurement values (0.38–3.53 kPa). Reliability values were consistently greater for superficial than for deeper muscles. (E-mail: francois.hug@ univ-nantes.fr) Ó 2015 World Federation for Ultrasound in Medicine & Biology. Key Words: Physiotherapy, Shear wave elastography, Shear modulus, Ultrasound, Electromyography.

address a specific aspect of spinal control during its performance (Hodges et al. 2013). As both techniques involve the development or refinement of a fine motor skill, the efficacy of the rehabilitation protocol may depend on the ability of the patient to accurately perform the task. To this end, a real-time, non-invasive measure to quantify individual muscle tension may benefit clinical practice. For both research and clinical practice, techniques such as electromyography (EMG) and B-mode ultrasound may be used to indirectly provide this information. However, there are several limitations to these techniques that require consideration. First, fine-wire EMG is invasive and, therefore, not applicable in clinical routine. Second, non-invasive surface EMG recordings are affected by cross-talk and cannot be used to isolate the activity of small or deep muscles (Farina et al. 2006). Third, the amplitude of EMG is influenced by many nonphysiologic factors such as placement of electrodes in relation to muscle fiber direction and electrical noise from the environment (Farina et al. 2006). Finally, the relationship between muscle architecture (thickness or length) measured with ultrasound and force is not linear (Brown and McGill 2010), which makes it difficult to

INTRODUCTION Rehabilitation strategies that include trunk stability exercises are associated with improved outcomes in individuals with low back pain (LBP) (Macedo et al. 2009). To this end, a variety of tasks that differentially target trunk muscle activation are commonly used. The abdominal hollowing technique is commonly thought to preferentially recruit the transversus abdominis (TA). This may be important, as the TA contributes to the control of spinal motion (Hodges et al. 2003; Kaigle et al. 1995), and differences in the behavior of this muscle have been observed in people with a history of LBP (Hodges 1999; Hodges and Richardson 1996). Alternative approaches to muscle retraining forego the intention to independently contract specific trunk muscles, with the intention to increase torso stiffness through trunk flexor and extensor muscle co-contraction (Hodges et al. 2013; McGill 2007) or abdominal bracing (Grenier and McGill 2007). Each rehabilitation protocol is thought to Address correspondence to: Franc¸ois Hug, UFR STAPS, University of Nantes, Nantes, F-44000, France. E-mail: francois.hug@ univ-nantes.fr D. MacDonald and A. Wan contributed equally to this work. 1

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accurately infer a change in muscle tension from a change in muscle architecture. A real-time ultrasound shear wave elastography technique, called supersonic shear imaging (SSI), can be used to accurately measure shear modulus (i.e., stiffness) of a localized muscle region (Lacourpaille et al. 2012). Previous studies have reported that the muscle shear modulus measured using SSI is linearly related to both active (Ates et al. 2015; Bouillard et al. 2011) and passive (Hug et al. 2015; Maisetti et al. 2012) muscle force. As a result, measurements of changes in muscle shear modulus during isometric contractions can be used to estimate changes in individual muscle force (or tension) (Hug et al. 2015; Sasaki et al. 2014). Elastography presents a unique method of assessing spinal stability exercises by providing a real-time index of individual muscle tension. However, before this technique is used in clinical practice, it is important to quantify the reliability of shear modulus measurements in abdominal muscles. Unlike work completed in superficial limb muscles (Lacourpaille et al. 2012), factors such as the depth of the trunk muscles, subcutaneous fat layer and respiratory movements are likely to affect the quality of the measurements. The aim of the present study was to assess the intrasession and inter-rater reliability of shear modulus measured in the abdominal muscles during two commonly used trunk stability exercises, the abdominal hollow and abdominal brace tasks. Muscle shear modulus was measured using SSI. METHODS Participants Thirty healthy volunteers participated in the study (16 males, 14 females; age 20 6 3 y, height 170 6 9 cm, weight 62 6 12 kg, body mass index [BMI] 21.2 6 2.8 kg/m2). Participants were informed in detail of the purpose of the study and the methods used, and provided informed written consent. Participants with a history of low back pain that had required musculoskeletal rehabilitation by a physiotherapist, current musculoskeletal pain on lying or abdominal surgery in the prior 24 mo were excluded from the study. None of the participants had experience with either of the two stability trunk exercises. Only one participant did not complete both trunk stability exercises (29 participants completed the abdominal hollowing and 30 completed the abdominal bracing). This study received ethical approval from the University of Queensland Human Ethics Unit. Examiners Two physiotherapy students (A.W. and M.M.) who had not previously used SSI served as the examiners for

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this reliability study. Before testing, both examiners underwent 20 h of practical training with co-investigator F.H., who has extensive experience with the SSI technique. Instrumentation Electromyography. Surface electromyographic activity was recorded by electrodes placed over the right obliquus externus abdominis (EO) and the right obliquus internus abdominis (IO). Two pairs of self-adhesive Ag/ AgCl electrodes (Blue Sensor N, Ambu, Copenhagen, Denmark) were placed over the right EO, inferior and medial to the 12th rib, and the right IO, medial to the anterior superior iliac spine (Fig. 1). A reference electrode was placed over the 10th thoracic vertebra. Skin was prepared using abrasive gel (Nuprep, D. O. Weaver, Aurora, CO, USA) and alcohol. EMG signals were pre-amplified 1000 times, bandpass filtered (20–500 Hz), notch filtered (50 Hz) and sampled at 1 kHz using a Power1401 Data Acquisition System with Spike2 software (Version 7.09a, Cambridge Electronic Design, Cambridge, UK). Electromyographic amplitude (displayed on a feedback screen as a percentage of the participant’s maximal voluntary contraction [MVC]) was monitored by the examiner during the training period and was used to direct verbal instructions to the participants regarding level of abdominal muscle activation. Elastography. An Aixplorer ultrasound scanner (Version 8.1.1, Supersonic Imagine, Aix en Provence, France), coupled with a linear transducer array (2–10 MHz; SuperLinear 10-2, Vermon, Tours, France) was used in the shear wave elastography mode (general preset) to measure shear modulus (Bercoff et al. 2004) of the four anterior trunk muscles: EO, IO, TA and rectus abdominis (RA). The ultrasound transducer was

Fig. 1. Surface electromyography electrode placement for obliquus externus abdominis (EO) (top) and obliquus internus abdominis (IO) (bottom).

Abdominal muscle stiffness reliability d D. MACDONALD et al.

positioned within the direction of the muscle fibers for each muscle (Drake et al. 2014) and perpendicularly to the skin (Fig. 2). The 2-D maps of muscle shear modulus were captured at 1 sample/s with a spatial resolution of 1 3 1 mm. Protocol Measurements of muscle shear modulus were taken at rest and during two modes of submaximal isometric contraction: an abdominal hollowing maneuver, intended to independently contract TA, and an abdominal bracing maneuver, aimed at increasing torso stiffness through trunk flexor and extensor muscle co-contraction. In an effort to increase the potential for the exercises to be performed using a repeatable strategy within and between participants, the normalized electromyographic amplitude of EO or IO was used to monitor the task’s intensity for the abdominal brace and abdominal hollow tasks, respectively. First, MVCs were performed in a semi-supine posture with shoulders in 90 flexion, hands clasped, knees in 90 flexion and feet flat on the bed shoulder width apart (Fig. 3). During the MVC, one investigator

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applied a trunk rotation force to the upper limbs, and another investigator maintained the legs. Participants were instructed to maximally resist the manual trunk rotation force that was applied by the investigators for 3 s. The MVCs were performed in both directions during separate trials, with 1-min intervals to allow for recovery. The maximum root-mean-square (RMS) EMG values of EO and IO over the six MVCs were considered to be the maximal activation of these muscles (RMS EMGmax). After a standardized 10-min instruction period (described in detail below), participants performed the stability trunk exercises. Throughout this period, participants were in a semi-supine posture with knees in 90 of flexion and feet flat on the bed, shoulder width apart. A series of three abdominal hollowing maneuvers and a series of three abdominal bracing maneuvers were performed twice, allowing two investigators to acquire the elastography data. Approximately 2 min of rest was provided between series of exercise maneuvers. During each repetition of the maneuvers, which were held for 30 s, data were acquired from the four test muscles. The order of investigator, maneuver and muscle was randomized for each participant.

Fig. 2. Ultrasound probe position for (a) obliquus externus abdominis, (b) obliquus internus abdominis, (c) transversus abdominis and (d) rectus abdominis.

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maximal RMS EMG values determined as described above. The mean RMS EMG values of EO and IO across each contraction were used to assess the intra-session variability. Only values measured by M.M. were then used to assess intra-session EMG variability. EMG variability was used to assist in the interpretation of the reliability outcomes of the muscle shear modulus. If within-subject variability of EMG is low between repetitions, it increases our confidence that the muscle shear modulus reliability outcomes are due to the muscle shear modulus measure, and not the repeatability of the task performance; the opposite is also true.

Fig. 3. Participant position: Supine crook, lying with knees flexed 90 .

For the abdominal brace task, participants were asked to simultaneously contract the abdominal and paraspinal muscles (i.e., ‘‘to contract the abdominal muscles as if they were preparing to resist against a physical impact to the abdomen’’). The target electromyographic amplitude for this maneuver was 10% of EO RMS EMGmax. Although some authors suggest a bracing contraction level of 25% RMS EMGmax for optimal torso stiffness (Brown and McGill 2005; McGill 2006), the bracing level was set at 10% RMS EMGmax to limit the effects of fatigue and breathing interferences on task performance (Hall et al. 2009). For the abdominal hollow task, participants were asked to draw the lower abdomen in toward the spine (i.e., to ‘‘draw the umbilicus toward the spine’’ and ‘‘draw the lower abdomen away from the waistband’’). For this task, the EMG amplitude target was set at 5% of IO RMS EMGmax. This goal was set based on the assumptions that TA is synergistic in its activation with IO (Newcomer et al. 2002) and that low levels of contraction are optimal for motor control training in LBP (Richardson et al. 2002; Tsao and Hodges 2007). Considering that the goal of rehabilitation is to retrain selective TA contraction and then to progress to contraction within functional tasks, this target is appropriately set at the boundary between independent TA activation (,5% RMS EMGmax) and functional activation levels (5%–20% RMS EMGmax) (Davidson and Hubley-Kozey 2005). Data analysis Electromyography. All EMG data were processed with Spike2 software (Version 7.09a, Cambridge Electronic Design, Cambridge, UK). For each contraction, the RMS EMG amplitude was calculated over 5 s at the middle of the task. These values were normalized to the

Elastography. All data were processed with MATLAB (The MathWorks, Natick, MA, USA). Videos of shear modulus maps were exported from the software (Version 8.1.1, Supersonic Imagine, Aix-en-Provence, France) in avi format and sequenced in jpeg format. A region of interest was defined for each map as the largest muscle area that avoided fascia, bone and hypo-echoic regions (Bouillard et al. 2014) (Fig. 4). Each jpeg image was visually inspected for artifacts. If any artefact or missing values (unfilled region within the elasticity map) were present, the measurement was discarded. Image processing converted each pixel of the color map into a value of the shear modulus based on the recorded color scale (Hug et al. 2014; Tucker et al. 2014), and the shear modulus was averaged over the region of interest on each image. Then, a single value was obtained by averaging the images (recorded at 1 sample/s) during each contraction (Hug et al. 2014; Tucker et al. 2014). This value was used for intra-session reliability measures. Given the good inter-rater reliability (reported in the Results), only values measured by M.M. were used to assess the intra-session reliability. A mean shear elastic modulus value across three contractions was calculated for each muscle for use in inter-rater reliability measures. In addition, we calculated the thickness of the superficial fat layer on the B-mode images aimed at measuring the RA muscle. This information was used to determine whether the thickness of the superficial fat layer influences the reliability of the muscle shear modulus. Statistics As proposed by Hopkins (2000), the intra-session variability of EMG and inter-rater reliability and intrasession reliability of shear modulus values were assessed using intra-class correlation coefficients (ICC) (ICC[3, 1] and ICC[3, 3] for intra-session reliability/variability and inter-rater reliability, respectively), the standard error of measurement (SEM) and the coefficient of variation (CV).

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Fig. 4. Example of shear modulus maps for (a) obliquus externus abdominis, (b) obliquus internus abdominis, (c) transversus abdominis and (d) rectus abdominis. The polygon on the shear elastic modulus map represents the region of interest used for data analysis.

RESULTS Reliability Electromyography. The variability of task performance was investigated by assessing the variability in EO and IO RMS EMG during the abdominal bracing and abdominal hollowing techniques, respectively. The mean EO EMG was 9.0 6 2.3% RMS EMGmax during abdominal bracing and the mean IO EMG was 4.6 6 1.4% RMS EMGmax during abdominal hollowing, compared with the intended target activity of 10% EO RMS EMGmax and 5% IO RMS EMGmax. Overall, both

tasks were accurately performed. When considering EO for the abdominal bracing task and IO for the abdominal hollowing task, intra-session ICC values were greater than 0.85 and SEM and CV values were correspondingly low (SEM ,0.95% RMS EMGmax; CV ,13.9%) (Table 1). Note that when the muscles were not used as a feedback (EO for abdominal hollowing and IO for abdominal bracing), they were more variable between the contractions (Table 1). Elastography. For each muscle, the intra-session and inter-rater reliability of shear modulus values measured

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Table 1. Variability of the normalized EMG amplitude values measured during the two different abdominal activation strategies Abdominal brace (n 5 30)

Electromyography Mean (% RMS EMGmax) Standard deviation Intra-session variability Intra-class correlation coefficient Standard error of measurement (% RMS EMGmax) Coefficient of variation (%)

EO

IO

9.0 2.3

8.6 7.4

0.86 0.95

0.96 1.55

1.1 6 0.4 cm; p 5 0.019). For BMI, similar trends were observed, with the presence of artifacts associated with greater participant BMI (IO: 22.6 6 2.7 kg/m2 vs. 20.5 6 2.6 kg/m2, p 5 0.054; TA: 22.8 6 2.9 kg/m2 vs. 20.6 6 2.5 kg/m2, p 5 0.007). DISCUSSION

11.1

19.2 Abdominal hollow (n 5 29)

Electromyography Mean (% RMS EMGmax) Standard deviation Intra-session variability Intra-class correlation coefficient Standard error of measurement (% RMS EMGmax) Coefficient of variation (%)

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EO

IO

5.7 3.7

4.6 1.4

0.87 1.59

0.85 0.62

20.9

13.9

n 5 number of participants for whom data were obtained for each muscle and task; EMG 5 electromyography; RMS 5 root mean square; EO 5 obliquus externus abdominis; IO 5 obliquus internus abdominis.

during the abdominal hollow and the abdominal brace was assessed. Because of measurement artifacts within the elasticity maps (absence of elasticity measurements or small region(s) of saturated values), IO and TA data were not analyzed for 11 (36.7%) and eight (26.7%) participants, respectively. For the remaining participants, fair to excellent intra-session and inter-rater reliability was observed with moderate to high ICC values (0.45–0.97), low to moderate SEM values (0.38– 3.53 kPa) and correspondingly low to moderate CV values (4.5%–28.7%) (Table 2). Note that intra-session reliability for TA at rest before hollowing maneuvers was low (ICC 5 20.03, SEM 5 1.35 kPa, CV 5 30.8%). Intra-session reliability was similar for the abdominal brace and the abdominal hollow. However, inter-rater reliability was greater in the abdominal hollow than in the abdominal brace. It should be noted that reliability values were consistently greater in EO and RA (superficial muscles) compared with IO and TA (deeper muscles). The possibility that body fat influences the reliability of the deepest muscles (IO and TA) was considered. The superficial fat layer was significantly thicker for participants for whom artifacts were observed than for the remaining participants (IO: 1.6 6 0.3 cm vs. 1.1 6 0.4 cm, p 5 0.007; TA: 1.6 cm 6 0.4 vs.

The aim of the study was to assess the intra-session and inter-rater reliability of shear modulus measurements in four abdominal muscles during two specific rehabilitation tasks. The reliability of successfully imaged muscles (between 63.3% and 100% of the participants, depending on the muscle) ranged from fair to excellent. Shear modulus measurements were more reliable for superficial muscles (EO and RA) than for deeper muscles (IO and TA). These results suggest that SSI may be used to provide real-time feedback on abdominal muscle tension during trunk stability exercises. Compared with surface EMG, this technique has the advantages of (i) being selective, as the measurement is not contaminated by cross-talk, and (ii) providing information on deep muscles for the majority of the participants. Further developments of the SSI technique are likely to improve the quality of measurements for deeper muscles. Lacourpaille et al. (2012) reported the excellent intra-session (ICC 5 0.81–0.95), inter-session (ICC 5 0.69–0.92) and inter-rater (ICC 5 0.42–0.94) reliability of the SSI technique in measuring shear modulus in nine resting upper and lower limb muscles. Both the intra-session reliability and inter-rater reliability reported in the present study are consistently lower than those reported by Lacourpaille et al. (2012). This difference is likely explained by muscle location (superficial limb muscles in Lacourpaille et al. [2012] versus both superficial and deep muscles herein) and muscle state (rest in Lacourpaille et al. [2012] versus both rest and contraction herein). Furthermore, abdominal muscle movements related to breathing may have affected the reliability of the elastography measurements both at rest and during contraction. Finally, it is important to note that the reliability assessed during the trunk stability exercises includes both the inherent variability of the measure and the variability in the way the participants performed the task. This is supported by the lower CV values found at rest than during contraction (except for TA) (Table 2). The variability in the way the participants performed the task can be indirectly assessed from EMG measurements of abdominal muscle during the study (Table 1). Interestingly, when EO RMS EMG was used to provide instructions to the participants (abdominal brace), the CV of EO RMS EMG (11.1%) was comparable to the CV of EO shear modulus (13.0%). This strongly suggests that the variability of the shear modulus measurements was

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Table 2. Reliability of shear modulus values measured in the four abdominal muscles during the two different abdominal activation strategies Abdominal brace EO (n 5 30)

Shear modulus Mean (kPa) SD (kPa) Intra-session reliability ICC SEM (kPa) CV (%) Inter-rater reliability ICC SEM (kPa) CV (%)

IO (n 5 20)

TA (n 5 22)

RA (n 5 29)

Rest

Contract

Rest

Contract

Rest

Contract

Rest

Contract

7.2 2.2

11.6 4.7

3.6 0.8

11.1 7.5

3.7 1.1

7.7 4.6

6.1 1.7

10.0 5.6

0.89 0.79 10.2

0.91 1.56 13.0

0.61 0.58 16.9

0.82 3.53 28.7

0.45 0.99 21.4

0.90 1.62 28.1

0.82 0.78 13.8

0.87 2.18 20.2

0.80 0.92 13.2

0.75 2.33 20.3

0.62 0.49 15.8

0.88 2.60 20.6

0.05 1.15 27.2

0.88 1.53 16.5

0.89 0.66 10.4

0.83 2.41 23.2

Abdominal hollow EO (n 5 29)

Shear modulus Mean (kPa) SD (kPa) Intra-session reliability ICC SEM (kPa) CV (%) Inter-rater reliability ICC SEM (kPa) CV (%)

IO (n 5 19)

TA (n 5 22)

RA (n 5 28)

Rest

Contract

Rest

Contract

Rest

Contract

Rest

Contract

6.9 2.1

7.6 2.0

3.5 0.9

6.0 3.0

4.0 0.8

5.4 1.8

5.4 1.8

6.2 2.1

0.87 0.81 13.0

0.86 0.85 11.9

0.58 0.77 24.3

0.82 1.46 25.5

20.03 1.35 30.8

0.60 1.41 24.6

0.90 0.64 14.4

0.80 1.06 17.5

0.96 0.39 4.5

0.97 0.38 4.6

0.86 0.39 13.4

0.88 1.01 13.3

0.68 0.50 15.2

0.85 0.74 11.6

0.91 0.57 11.0

0.92 0.61 10.1

n 5 number of participants for whom data were obtained for each muscle and experiment; SD 5 standard deviation; ICC 5 intra-class correlation coefficient; SEM 5 standard error of measurement; CV 5 coefficient of variation; EO 5 obliquus externus abdominis; IO 5 obliquus internus abdominis; TA 5 transversus abdominis; RA 5 rectus abdominis.

attributable mainly to the variability of the task, at least for this superficial muscle during this task. The deeper muscles of the abdominal wall (IO and TA) provided greater methodologic challenges than the superficial muscles. All maps were visually inspected, and poor-quality shear modulus maps were discarded. This was more often the case for people with higher BMI and, therefore, thicker superficial fat layers (albeit within a healthy BMI range). The reduced quality of these images is likely due to a significant reduction in propagation velocity of the sound waves within fat tissue (about 1450 m/s) compared with other tissues (e.g., muscle: 1580 m/s). As a close match between the actual and expected sound wave velocities is critical to generation of the shear waves, a thicker fat layer between the probe and the targeted tissue can interfere with the generation of shear waves within the target tissue and may lead to the inability of the technique to measure shear wave velocity, that is, unfilled maps of elasticity or artifacts/ saturated values. Interestingly, this reduction in image quality was only in recordings of the deep muscles

and only in about one-third to one-fourth of the participants for IO and TA, respectively. For the majority of the other participants, both intra-session reliability and inter-rater reliability were fair to excellent (except for TA at rest). Although an increase in muscle tension was observed in all muscles during the brace and in TA and IO during the hollow, large within-subject variability was observed (Table 2). This inter-subject variability may be explained by differences in the motor strategies used between individuals despite standardized instructions and cues. If that is the case, the use of an additional measure, such as SSI, to quantify muscle tension and to provide real-time feedback to the patient may offer some benefit in clinical practice. As mentioned in the Introduction, the main advantage elastography has compared with EMG or B-mode ultrasound is that it provides a more direct assessment of muscle tension. In addition, SSI is easy to use and does not require extensive training; 20 h of practical training was sufficient to achieve good inter-rater reliability.

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The present study requires the consideration of several limitations. First, to minimize the invasiveness of the procedure, the protocol used surface EMG to standardize the contraction intensity. This presents problems with cross-talk and a lack of specificity, particularly for the channel intended to record the electrical activity of IO. Also, the present study offers important information only on the repeatability of SSI measures on the same day. Therefore, the results cannot be generalized to inter-session reliability. However, the main motive for using elastography is to provide real-time feedback to the participants, and within this context the intra-session reliability is more important than the inter-session reliability. Acknowledgments—The authors thank Will Hopkins (Auckland University of Technology, New Zealand) for his statistical advice during revision of the article. This study was supported by the Region Pays de la Loire (QUETE project, no. 2015-09035).

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