Musculoskeletal Science and Practice 32 (2017) 57e63

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Original article

Ultrasound imaging transducer motion during standing postural tasks with and without using transducer fixator F. Ehsani a, M. Salavati b, *, A.M. Arab b, *, M.H. Dolati c a

Neuromuscular Rehabilitation Research Center, Semnan University of Medical Sciences, Semnan, Iran Department of Physical Therapy, University of Social Welfare and Rehabilitation Sciences, Tehran, Iran c Biomedical Engineering Department, Kosar Hospital, Semnan University of Medical Sciences, Semnan, Iran b

a r t i c l e i n f o

a b s t r a c t

Article history: Received 1 February 2017 Received in revised form 8 June 2017 Accepted 23 August 2017

Background: Changes in the orientation of ultrasound (US) transducer relative to the body surface during dynamic standing tests can affect US measurements. Objective: The purpose of the study was to evaluate ultrasound imaging transducer motion while measuring the lateral abdominal muscle thickness during standing tasks with and without using transducer fixator (TF). Design: Cross-sectional experimental study. Methods: A digital optical motion analysis system was used to assess the motions of US transducer during double-leg stance in different levels of platform stability of Biodex Balance System (BBS) (static, levels 6 and 3) with and without using TF in 45 healthy individuals. In addition, lateral abdominal muscle thickness was evaluated by US imaging. Results: The results indicated that the amount of angular and linear transducer motions during static and dynamic standing tasks significantly decreased by the use of TF as compared to the conditions without TF (P < 0.001, effect size> 0.84). Conclusion: TF can significantly control US transducer motions within acceptable threshold limits during standing postural task. This may improve the clinical application of US imaging. © 2017 Elsevier Ltd. All rights reserved.

Keywords: Ultrasound imaging Ultrasound transducer motion Standing task Transducer fixator

1. Introduction Clinical applications of ultrasound (US) imaging in order to measure muscle function by physiotherapists are increasing (Teyhen, 2006). Although needle electromyography (NEMG) is one of the most accurate methods for the assessment of trunk muscle activity (Hodges and Richardson, 1998; Hodges, 2001), it is not always a practical and safe technique. This may be especially true in clinical setting. Therefore, real-time US imaging has been introduced in an attempt to provide a safe, cost-effective and feasible method for the assessment of deep and superficial muscles' function (Costa et al., 2009; McMeeken et al., 2004; Teyhen et al., 2007). There is strong evidence supporting the validity and reliability of US for the measurement of lateral abdominal muscles' function (Ferreira et al., 2004; Costa et al., 2009; Kiesel et al., 2008; Hebert

* Corresponding authors. E-mail addresses: [email protected] (F. Ehsani), mahyarsalavati@ gmail.com (M. Salavati), [email protected] (A.M. Arab). http://dx.doi.org/10.1016/j.msksp.2017.08.009 2468-7812/© 2017 Elsevier Ltd. All rights reserved.

et al., 2009; Kidd et al., 2002; Koppenhaver et al., 2009). McMeeken et al. (2004) have shown significant correlations between the NEMG recordings of the transverse abdominis (TrA) muscle activity and US data, as examined by muscle thickness changes. Thus, US imaging seems to be a non-invasive and appropriate alternative for assessment of abdominal muscle function. Any change in the orientation of US transducer relative to the body surface has been observed to be a potential source of errors caused by muscle image distortion (Dupont et al., 2001; Reddy et al., 2001; Klimstra et al., 2007). This may affect measurement results, particularly when US is used during dynamic standing tests (Dupont et al., 2001; Reddy et al., 2001; Klimstra et al., 2007). In this regard, some studies have suggested the error threshold guidelines for US transducer motion below which US imaging measures are not affected during semi-dynamic clinical tests in supine position (Whittaker et al., 2009, 2010). Standing positions such as walking, running and, stair climbing are believed to be responsible for the development of pain in some individuals with musculoskeletal disorder, especially patients with low back pain (LBP) (Van Deursen et al., 2002). Owing to the importance of trunk muscle function

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assessment during dynamic standing tasks, providing standardized procedures for controlling US transducer motions may be beneficial in order to improve the clinical applications of US imaging. Accordingly, some studies have used transducer fixator (TF) to stabilize US transducer during dynamic tasks (Bunce et al., 2002, 2004; Kim et al., 2013). However, no study has investigated the effects of TF on the amount of US transducer displacement during standing postural tasks. To the best of the authors' knowledge, only one study has compared the reliability of US measures of lateral abdominal muscle thickness during standing postural tasks in conditions with and without TF (Ehsani et al., 2016a). The results showed higher reliability levels of US imaging when TF was used (Ehsani et al., 2016a). Therefore, one of the aims of the present study was to compare US transducer motions during the measurement of lateral abdominal muscles' thickness while standing on different unstable surfaces with and without using TF. Our other objective was to evaluate the relationship between US transducer motions and muscle thickness measures obtained by US imaging. It was hypothesized that: 1. TF limits the US transducer motions during the assessment of lateral abdominal muscles' thickness in standing postural tasks. 2. US transducer motions affect the US muscle thickness measures when TF is not used.

2. Materials and methods 2.1. Study design and ethical approval statement In this cross-sectional experimental study, the amount of the US transducer motion was compared in the conditions with and without TF. The study was approved by the Human Research Ethics Committee at the XXX (Ethics Code: USWR.REC.1393.148). In addition, the study protected the rights of all participants. All subjects signed a consent form before participation. 2.2. Participants Fifty-five healthy participants were selected through convenient non-probability sampling. Of these, 45 subjects (22 females and 23 males) completed the tests and their data were used for statistical analysis. At the significance level of 0.05, the sample size showed a power of 0.85 to detect changes in the US transducer displacement. The flowchart of eligibility assessment throughout the study is represented in Fig. 1. Participants were recruited among university students and staff. They were excluded if they had a history of back pain and respiratory disorder. In addition, people with visual, vestibular, auditory or cognitive impairments, as well as diabetes, recent lower limb pathology, pregnancy and a history of recent use of any medication or substance affecting their balance during 48 h prior to testing were excluded. 2.3. Experiments 2.3.1. US imaging protocol An US unit (HS-2100 V, Honda Electronics Co, Toyohashi Aichi, Japan) set in B-mode with a 7.5 MHz linear head transducer was used in order to measure lateral abdominal muscle size. Imaging was performed on the right side of the abdominal wall. In order to capture TrA, internal oblique (IO) and external oblique (EO) muscles, the transducer was placed over anterior axillary line, midway between the 12th rib and the anterior superior iliac crest (Ehsani et al., 2016b). The location showing the clearest image of the

Fig. 1. Flow diagram of participant's eligibility assessment.

above-mentioned muscles was marked for standardized transducer placement across all test conditions. The reference point for abdominal muscle thickness measurement in each image was carefully calculated between the inner edge of each muscle fascial bands from 2 cm (cm) lateral to the v-shaped medial border of TrA muscle in each image (Ehsani et al., 2016b; Vasseljen and Fladmark, 2010). Both techniques provide acceptable data but the reliability has been shown to be higher with the use of TF (Ehsani et al., 2016a). Therefore, the US imaging with and without TF was assumed to be reliable enough to be compared in the present study (Ehsani et al., 2016a). The TF consisted of a custom made high-density foam and an elastic belt (Fig. 2). 2.3.2. Biodex Balance System protocol A Biodex Balance System (BBS) (950-302, SD, Biodex Co., New York, USA) was used for simulating the conditions of static and dynamic standing postural tasks. BBS evaluates a participant's balance while standing on a movable platform with varying degrees of surface instability (with levels 1 and 12 as greatest and smallest instability, respectively) (Hinman, 2000). The participants were asked to stand barefoot with their hands crossed behind their back for 30 s. They were instructed to maintain the platform of the BBS level without holding its handrails while looking at a paper on a wall 2 m (m) in front of their eyes (Fig. 3 a, b). 2.3.3. Motion analysis system protocol To monitor the motions of US transducer during standing test conditions, a digital optical motion analysis system with seven cameras and sampling frequency of 120 Hz (Qualysis AB, Qualysis Co., Gothenburg, Sweden) was used. In an attempt to achieve below 1 mm (mm) measurement error for the system, the cameras were set in capture volume of approximately 2 m width, 2 m length and 2 m height (Whittaker et al., 2010). Four retro-reflective markers (14 mm in diameter) were attached to left and right anterior superior iliac crest spines (ASIS), as well as Xiphoid process and the 6th rib in line of the Xiphoid process. These markers were used to define a reference trunk frame formed by right ASIS, right 6th rib

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Fig. 4. Axes of US transducer motion on the body surface in the lateral abdominal region during standing tests. Fig. 2. Different components of transducer fixator.

and Xiphoid (modulation method of Kadaba et al., study (1990) and Armand et al., study (2014)). In the testing conditions with TF, two retro-reflective markers were vertically placed at the end of the US transducer and two additional markers were horizontally placed on the superior lateral surface of TF foam (Fig. 3a). In the testing conditions without TF, two retro-reflective markers were vertically placed at the end of the US transducer and two other markers were horizontally placed on the superior surface of the US transducer (Fig. 3b). The kinematic data captured during static standing test on the BBS platform with and without TF were used for instrument calibration. According to Whittaker et al. (2010), a kinematic model was designed in MATLAB software (version 7.10.0.499, The Mathworks Co., Massachusetts, USA) to define the trunk and US transducer segments and determine the rotation and displacement of the transducer with respect to the trunk segment (Whittaker et al., 2010). With this local coordinate system model, the angular motions of the US transducer related to the trunk segment, in degrees, were considered around X (clockwise/counter clockwise; CW/ CCW), Y (cranial/caudal tilt of the proximal end of the transducer) and Z (medial/lateral tilt of the proximal end of the transducer) axes

(Fig. 4) (Whittaker et al., 2010). The calculation of the three rotations of the US transducer related to the trunk segment was performed based on Eulery system sequences (XY'Z00 ) (Whittaker et al., 2010). Additionally, the linear translation, in mm, was measured from the transducer's markers relative to the trunk segment in X axis (inward and outward motion). 2.4. Experimental procedure Six test conditions, including 3 levels of postural condition (BBS static, 6 and 3 levels) and 2 levels of transducer condition (with and without TF) with a 5-min inter-trial interval were completed by each participant. The motion analysis system was calibrated at each session prior to testing. The kinematic data collected by the motion analysis system were saved in the form of a MATLAB file. Concurrently, the US imaging data from each 30-s test trial were transferred to a personal computer to be processed offline (Ehsani et al., 2016b). A code number was given to the data of each test condition by one examiner and two other blind examiners independently performed the processing of US and kinematic data. We assessed intra and inter-session reliability of motion analysis system measurement of US transducer displacements during

Fig. 3. a: Experimental setup of US imaging on lateral abdominal region in the condition of using transducer fixator (TF), while the retro-reflective markers imposed on the ASISs, Xiphoid, 6th rib, TF and on the ultrasound transducer. Fig. 3, b: Experimental setup of US imaging on lateral abdominal region in the condition of absence transducer fixator (TF), while the retro-reflective markers imposed on the ASISs, Xiphoid, 6th rib, and on the ultrasound transducer.

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standing test conditions in healthy participants. In this reliability study, each test condition was randomly repeated four times at each session in the same laboratory by the same examiner. Test and retest sessions of measurements were 3e5 days apart. Data collection was performed from September 2015 to January 2016. The study was conducted based on the STROBE checklist criteria. 2.5. Data analysis Kolmogrov-Smirnov (K-S) tests were used to examine the normality of distribution for measured variables. All studied variables showed normal distribution (K-S p values higher than 0.05). To evaluate the reliability of motion analysis system, the twoway mixed model of intra-class correlation coefficients (ICCs) was used (Shrout and Fleiss, 1979). In order to conduct inter-session reliability analyses, one of the four scores of the transducer motion for each standing test condition per session was randomly selected. ICC1,4 was used for inter-session reliability and ICC1,2 was calculated for intra-session reliability (Shrout and Fleiss, 1979). Moreover, paired t tests were conducted to detect any systematic bias between test and retest scores (Atkinson and Nevill, 1998). The error thresholds for the motions of US transducer were defined based on Whittaker et al., (2009). They suggested that US transducer angular motions around X and Y axes for TrA muscle thickness measurements should be < 9 and 0.05). Table 3 shows the paired t-test results for the amounts of angular and linear US transducer motion between conditions with and without TF. The findings showed significant differences for angular and linear US transducer motions between conditions with

and without TF (P < 0.001). The observed angular transducer displacements around X, Y and Z axes were significantly decreased by the use of TF during all standing tests (effect size (ES) > 0.84). In addition, the amounts of linear transducer motion (inward/outward direction) were significantly smaller in conditions with TF, as compared to conditions without TF (ES > 0.95). The results of Pearson correlation analyses indicated significant weak correlations between abdominal muscle thickness values and US transducer angular motion around Y axis as well as linear X translation in conditions without TF (Table 4). Additionally, the findings presented in Table 5 indicate significant differences of IO and EO muscle thickness during all standing tests between conditions with TF and without TF. 4. Discussion Our findings indicated that motion analysis system is a reliable tool for the assessment of US transducer motions in postural standing tasks, although the system is not used in clinical settings. The intra-session and inter-session ICCs ranged from 0.50 to 0.85 in conditions with and without TF. Although the reliability of motion analysis system for the assessment of US transducer motions in postural standing tasks had not been previously investigated, some reliability studies have reported similar ranges of reliability for motion analysis system (Mackey et al., 2005; Ross et al., 2015). Mackey et al. reported a range of inter-session ICCs of motion analysis system from 0.49 to 0.74 for kinematic measurement of upper and lower limbs movements during walking in hemiplegic patients (Mackey et al., 2005). In addition, Ross et al. (2015) found intra-session ICCs of motion analysis system ranging from 0.50 to 0.89 for kinematic measurement of lower limb joints in sagittal plan during walking in healthy individuals. According to the results, it seems that motion analysis system is a reliable tool for kinematic measurement of US transducer motions in standing tasks. It was hypothesized that the use of TF may limit the amount of US transducer motions during standing postural tasks. Results support the hypothesis and show that using TF significantly decreased US transducer motions during static and dynamic standing tests (ES > 0.8). Significant greater amounts of US transducer motion were observed during conditions without TF. Moreover, in conditions without TF, the defined error thresholds (Whittaker et al., 2009) were within 95%CIs of all transducer displacement amounts. This implies that in many cases the observed displacements were beyond these thresholds when TF were not used. Interestingly, in conditions with TF, even the maximum values of 95%CI for US transducer motions were lower than suggested error threshold (7.91 mm, 5.96 around X axis, 4.81 around Y axis and 7.91 around Z axis). Therefore, our results confirmed the considerable effects of TF in controlling linear and angular motions of US transducer during static and dynamic standing postural tasks. Large displacements of transducer during US imaging of dynamic clinical tests have been reported previously (Whittaker et al., 2009, 2010). Consequently, it was considered as a serious confounding variable which should be addressed in US measurements of muscle thickness (Dupont et al., 2001; Reddy et al., 2001; Klimstra et al., 2007). In this regard, controlling US transducer motion has been suggested to be essential for reliability and validity of US imaging. We found decreased amounts of US transducer motions to the levels below defined error threshold limits with the use of TF. This may be an evidence of successful control of this confounding variable. Therefore, as a clinical message, US imaging can be practiced during a wide variety of standing tests with acceptable reliability and validity levels, if TF is used. We also hypothesized that there is a relationship between the amount of US transducer motions and measured muscle thickness

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Table 1 Descriptive statistics of angular and linear US transducer motions during static and dynamic standing tests in the conditions with and without TF. TF state

Testing condition

X axis rotation, degree mean ± SD ( ) (95% CI)

Y axis rotation, degree mean ± SD ( ) (95% CI)

Z axis rotation, degree mean ± SD ( ) (95% CI)

X translation, mean ± SD (mm) (95% CI)

With

Static stance

1.23 ± 0.34 (0.16e4.02) 1.29 ± 0.23 (0.02e5.96) 1.19 ± 0.22 (0.03e4.01) 2.93 ± 0.52 (0.12e6.38) 3.68 ± 0.61 (0.23e16.92) 3.03 ± 0.24 0.21-11.36)

1.02 ± 0.22 (0.18e3.83) 1.23 ± 0.25 (0.01e4.81) 1.12 ± 0.13 (0.02e3.43) 2.88 ± 0.52 (0.02e7.30) 3.38 ± 0.23 (0.04e6.43) 2.94 ± 0.39 (0.23e11.57)

1.28 ± 0.28 (0.03e3.61) 1.33 ± 0.22 (0.12e4.84) 1.99 ± 0.33 (0.02e7.91) 3.08 ± 0.67 (0.03e7.33) 3.59 ± 0.14 (0.01e16.14) 2.90 ± 0.26 (0.13e11.61)

2.78 ± 0.45 (0.01e7.07) 3.16 ± 0.26 (0.11e7.91) 3.55 ± 0.39 (0.10e7.89) 6.86 ± 0.25 (0.02e17.92) 7.49 ± 0.80 (0.11e20.12) 7.89 ± 0.59 (0.01e22.45)

Dynamic stance, Level 6 Dynamic stance, Level 3 Without

Static stance Dynamic stance, Level 6 Dynamic stance, Level 3

TF: Transducer Fixator, SD: Standard Deviation, CI: Confidence Interval.

Table 2 Intra- and inter-session reliability of the motion analysis system measurements at different standing tests in the conditions with and without fixator. Stability Level

Static stance

TF state

With

Without

Dynamic stance, level 6

With

Without

Dynamic stance, Level 3

With

Without

Transducer motion direction

TrACh.X TrACh.Y TrACh.Z TrLD TrACh.X TrACh.Y TrACh.Z TrLD TrACh.X TrACh.Y TrACh.Z TrLD TrACh.X TrACh.Y TrACh.Z TrLD TrACh.X TrACh.Y TrACh.Z TrLD TrACh.X TrACh.Y TrACh.Z TrLD

Intra-session ICC (95% CI) Retest

Test

0.55 0.56 0.51 0.71 0.60 0.76 0.73 0.52 0.53 0.63 0.51 0.70 0.55 0.61 0.51 0.56 0.74 0.77 0.83 0.74 0.69 0.63 0.66 0.53

0.54 (0.22e0.71) 0.51 (0.28e0.68) 0.5 (0.24e0.66) 0.56 (0.35e0.71) 0.65 (0.48e0.77) 0.72 (0.59e0.82) 0.77 (0.65e0.85) 0.73 (0.61e0.82) 0.62 (0.45e0.74) 0.73 (0.61e0.82) 0.66 (0.51e0.77) 0.72 (0.60e0.81) 0.61 (0.41e0.74) 0.71 (0.58e0.81) 0.50 (0.26e0.68) 0.53 (0.30e0.71) 0.81 (0.73e0.87) 0.82 (0.74e0.88) 0.85 (0.79e0.90) 0.73 (0.61e0.83) 0.72 (0.52e0.88) 0.75 (0.63e0.84) 0.75 (0.63e0.81) 0.51 (0.23e0.67)

(0.22e0.74) (0.21e0.73) (0.23e0.67) (0.56e0.81) (0.41e0.74) (0.65e0.75) (0.60e0.83) (0.29e0.68) (0.43e0.65) (0.46e0.76) (0.28e0.68) (0.53e0.81) (0.32e0.71) (0.38e0.74) (0.27e0.66) (0.35e0.72) (0.62e0.83) (0.66e0.85) (0.75e0.89) (0.61e0.83) (0.51e0.82) (0.41e0.77) (0.46e0.79) (0.26e0.71)

Inter-session ICC (95% CI)

SEM

MMDC

CV

0.58 0.51 0.55 0.53 0.55 0.56 0.58 0.51 0.73 0.69 0.52 0.63 0.53 0.74 0.73 0.56 0.70 0.66 0.54 0.52 0.70 0.59 0.65 0.53

0.08 0.12 0.09 0.18 0.14 0.28 0.23 0.23 0.09 0.11 0.10 0.15 0.25 0.33 0.22 0.33 0.10 0.06 0.11 0.24 0.10 0.28 0.18 0.29

0.15 0.24 0.17 0.35 0.28 0.55 0.44 0.45 0.17 0.21 0.19 0.30 0.50 0.64 0.44 0.64 0.19 0.13 0.22 0.46 0.20 0.55 0.36 0.56

0.11 0.14 0.12 0.11 0.07 0.14 0.10 0.04 0.13 0.13 0.10 0.11 0.11 0.19 0.12 0.06 0.13 0.08 0.12 0.10 0.06 0.15 0.09 0.06

(0.30e0.85) (0.29e0.65) (0.25e0.69) (0.29e0.66) (0.28e0.72) (0.38e0.71) (0.33e0.74) (0.26e0.61) (0.63e0.89) (0.55e0.79) (0.22e0.65) (0.40e0.77) (0.26e0.77) (0.58e0.84) (0.58e0.83) (0.39e0.73) (0.53e0.81) (0.48e0.79) (0.31e0.68) (0.11e0.69) (0.53e0.81) (0.35e0.75) (0.44e0.78) (0.26e0.71)

Table 3 Paired t-test of the Ultrasound transducer motion between the conditions with and without transducer fixator. Transducer motion direction

TrACh.X (SS) TrACh.Y (SS) TrACh.Z (SS) TrACh.X (D6S) TrACh.Y (D6S) TrACh.Z (D6S) TrACh.X (D3S) TrACh.Y (D3S) TrACh.Z (D3S) Tr LD (SS) Tr LD (D6S) Tr LD (D3S)

With fixator

Without fixator

Mean

SD

Mean

SD

1.23 1.02 1.28 1.29 1.23 1.33 1.19 1.12 1.99 2.78 3.16 3.55

0.34 0.22 0.28 0.23 0.25 0.22 0.22 0.13 0.33 0.45 0.26 0.39

2.93 2.88 3.08 3.68 3.38 3.59 3.03 2.94 2.90 6.86 7.49 7.89s

0.52 0.52 0.67 0.61 0.23 0.14 0.24 0.39 0.26 0.25 0.80 0.59

Mean difference (95% CI)

P value

Effect size

1.50 1.86 2.10 2.39 2.15 2.26 2.04 1.82 0.91 4.08 4.33 4.34

Ultrasound imaging transducer motion during standing postural tasks with and without using transducer fixator.

Changes in the orientation of ultrasound (US) transducer relative to the body surface during dynamic standing tests can affect US measurements...
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