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Journal of Back and Musculoskeletal Rehabilitation 27 (2014) 339–347 DOI 10.3233/BMR-130453 IOS Press
Reliability of the ultrasound measurements of abdominal muscles activity when activated with and without pelvic floor muscles contraction Nahid Tahana,∗, Omid Rasoulib , Amir Massoud Arabc , Khosro Khademia and Elham Neisani Samanid a Department of Physical Therapy, Faculty of Rehabilitation Science, Shahid Beheshti University of Medical Sciences, Tehran, Iran b Department of Physical Therapy, Faculty of Health Education and Social Work, Sør-Trøndelag University College (HiST), Trondheim, Norway c Department of Physical Therapy, University of Social Welfare and Rehabilitation Sciences, Evin, Tehran, Iran d Taleghani Hospital, Shahid Beheshti University of Medical Sciences, Tehran, Iran
Abstract. BACKGROUND: Synergistic co-activation of the abdominal and pelvic floor muscles (PFM) has been shown in literature. Some studies have assessed the reliability of ultrasound measures of the abdominal muscles. OBJECTIVE: The aim of this study was to determine the reliability of ultrasound measurements of transverses abdominis (TrA) and obliquus internus (OI) muscles during different conditions (PFM contraction, abdominal hollowing manoeuvre (AHM) with and without PFM contraction) in participants with and without chronic low back pain (LBP). METHODS: 21 participants (9 with LBP, 12 healthy) participated in the study. The reliability of thickness measurements at rest and during each condition and thickness changes and percentage of this changes at different conditions were assessed. RESULTS: The results showed high reliability of the thickness measurement at rest and during each condition of TrA and OI muscles, moderate to substantial reliability for the thickness change and percentage of thickness change of TrA, and fair to moderate reliability of the thickness change and percentage of thickness change of OI in both groups. CONCLUSIONS: Ultrasound imaging can be used as a reliable method for assessment of abdominal muscle activity with and without PFM contraction. Keywords: Low back pain, pelvic floor muscles, abdominal muscles, reliability
1. Introduction Low back pain (LBP) is one of the most frequent complaints in today’s societies. Previous studies have indicated that 70–80% of the western population have had at least one episode of LBP in their lifetime [1]. ∗ Corresponding author: Dr. Nahid Tahan, Damavand Ave, Emam Hossein Square, P.O Box 1616913111, Tehran, Iran. Tel.: +98 21 77548496; Fax: +98 21 77561406; E-mail: nahidta2431@Gmail. com.
Several factors, based on clinical findings and scientific experiments, have been associated with the development of LBP. However, during the recent decades the main focus has been placed on segmental lumbar spine instability and its association with LBP. There is substantial evidence indicating that main impairment in patients with chronic LBP is deep local muscles dysfunction [2–4], which may affects spinal stability [5]. The deep antero-lateral abdominal muscles including transverse abdominis (TrA) and obliqus internus (OI) play an important role in providing spinal stability
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during functional activities [6,7]. Accordingly, during the past decade the main focus of rehabilitation program for patients with LBP has been placed on specific therapeutic exercises for key stabilizing muscles including deep abdominal muscles [8]. The abdominal hollowing maneuver (AHM) is commonly used to assess and rehabilitate the abdominal muscles [9–11]. The abdominal hollowing manoeuvre is performed to activate deep antero-lateral abdominal muscles [8]. This is achieved by instructing the participants to hollow their abdomen by drawing their navel up and in towards the spine [12]. Recent studies have led to understanding of the synergistic co-activation between the abdominal and pelvic floor muscles (PFM) for development of intraabdominal pressure and load transfer [13–15]. Electromyographic (EMG)studies have demonstrated that all the abdominal muscles are activated during voluntary contraction of the PFM [16,17]. However, normalized EMG activity was greater for OI and TrA than obliqus externus (OE) [18]. Accordingly, the PFM are generally accepted as a part of the trunk stability mechanism. PFM dysfunction has been reported in individuals with LBP compared with healthy subjects [19]. Ultrasound is a safe, cost-effective and accessible method for visualizing and measuring the deep muscles in real time manner [20], that allows direct visualisation of the abdominal muscles and can measure the change in thickness of a muscle as it contracts over the time. A variety of measurement tools have been used by physical therapists to assess the abdominal muscle functions in subjects with LBP attending physical therapy clinics. More recently, there is more interest in the use of real-time ultrasound imaging as valid method to evaluate muscle structure, function and activation patterns. The ultrasound imaging (UI) allows direct visualization for real time study of the muscles as they contract over the time. This is especially important when the deep abdominal muscle activity is investigated. Changes in the thickness of abdominal muscles are measured as an indicator of abdominal muscle activity during ultrasound imaging [21]. Validity studies have compared ultrasound measurements with EMG and found good to high correlation between measurements of muscle thickness and EMG activity at low activity levels [21,22]. However, these researchers found that OE behaved in a different way from TrA and OI and there was no consistent relationship between muscle thickness and EMG activity of OE. The reliability of this method for measuring changes in TrA mus-
Table 1 Demographic data for the Healthy and LBP groups Variables Age (year)
Group Healthy LBP
Mean ± SD 24.9 ± 3.8 26.5 ± 8.5
Minimum 21.00 18.00
Maximum 33.00 47.00
Weight (kg)
Healthy LBP
61.00 ± 10.4 61.3 ± 9.5
45.00 48.00
76.00 77.00
Height (cm)
Healthy LBP
160 ± 10 160 ± 5
150 155
183 171
22.1 ± 3.09 22.7 ± 2.2
18.7 19.9
28.5 26.6
BMI (Kg/m2 ) Healthy LBP
cle thickness has been assessed previously. Costa reported moderate reliability for thickness changes [23]. These findings support using of ultrasound imaging as a non-invasive technique to measure TrA and OI muscle thickness and estimate relative muscle activity when these muscles are voluntarily contracted. Although several studies have investigated the reliability of ultrasound measures of the abdominal muscles, most have investigated reliability during resting states or when the abdominal muscles contracted alone. To our knowledge, no study has directly investigated the reliability of ultrasound measurement of the abdominal muscle activity during contraction with and without PFM contraction so the purpose of this study was to evaluate the intra-examiner reliability of the ultrasound measurements of TrA and OI muscles at rest, during PFM contraction and during abdominal hollowing manoeuvre with and without PFM contraction in subjects with and without non-specific chronic LBP.
2. Materials and methods 2.1. Participants A total of 21 participants (9 with LBP, 12 healthy individuals) participated in the study. The subject population in this study was a sample of convenience made up of subjects who were between the ages of 18 and 47 years. Participants with LBP were selected among the patients visited in the orthopedic and physical therapy clinics. All the participants in the study filled out a simple health questionnaire. Those who met the selection criteria were included in the study. All the participants signed an informed consent form approved by the human ethics committee of university of Social Welfare and Rehabilitation Sciences. The demographic data of the participants are shown in Table 1.
N. Tahan et al. / Reliability of the ultrasound measurements of abdominal muscles activity 2.0
2.0
+1.96 SD 1.42
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+1.96 SD 1.38
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-0.5 -1.0
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-1.5 -1.96 SD -2.04
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-1.96 SD -1.82
-2.0 -2.5
-2.5 1.0
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2.0 2.5 3.0 3.5 AVERAGE of Test and Re-test
4.0
4.5
0
1
(a) LBP subjects
2 3 AVERAGE of Test and Re-test
4
5
(b) Healthy Subjects
Fig. 1. The Bland-Altman plot for ultrasound measurements of thickness at rest for TrA in LBPand healthy subjects.
Patients were included if they had a history of LBP for more than six weeks before the study or had on and off back pain and had experienced at least three episodes of LBP, each lasting more than one week, during the year before the study [24]. A visual analogue scale (VAS) was used to assess the pain intensity. VAS score of 2 or less on the day of test was considered as a further inclusion criterion. Healthy participants had no complaint of any pain or dysfunction in their low back, pelvis, thoracic and lower extremities. Participants were excluded if they had a history of surgery in the lumbar spine, radiculopathy, persistent severe pain, neurological symptoms, severe spinal instability, osteoporosis, structural deformity, systemic inflammatory disease, previous spinal fusion, severe cardiovascular diseases, acute infection, recent abdominal surgery and uncontrolled alcohol/drug abuse. A further exclusion criterion was pregnancy. 2.2. Ultrasound imaging A diagnostic ultrasound imaging unit set in B-mode (Ultrasonix-ES500, Canada) with a linear array transducer (7.5 MHz) was used to measure the abdominal muscle thickness at rest, during PFM contraction and during abdominal hollowing manoeuvre with and without PFM contraction based on the method explained by others [22,25–28]. The measurements were made on the right side of the abdominal wall. The participants were tested in crook-lying position with one pillow underneath the head and knees. The lumbar spine was positioned in neutral. The skinwas marked to confirm the exact po-
sition of the transducer on the abdominal wall. The transducer was transversely located across the abdominal wall, 25 mm antero-medial to the midway point between the 12th rib and the iliac crestover the anterior axillary line to obtain a clear image of the deep abdominal layers [22]. The ultrasound transducer was not displaced during the testing procedure. Actual muscle thicknesses (TrA, OI) at rest (end of expiration) and during contractions (PFM contraction, abdominal hollowing manoeuvre with and without PFM contraction) were measured. The cursor points carefully measured the muscle thickness between the inside edge of fascial bands in millimetres (mm) (Fig. 1). The maximum thicknesses at rest and during each contraction for the abdominal muscles (TrA, OI) were calculated. 2.3. Procedures The participants were assessed two times for intratester reliability of the ultrasound measurements. For this purpose, at first the examiner performed the measurements in participants, and then repeated the measurements after 30 minutes in a blinded fashion and random order with the same procedure. The participants were allowed to get up, walk around and be active during 30 minutes rest. Prior to testing, participants were trained by a physiotherapist to perform the abdominal and PFM contractions correctly using ultrasound as a biofeedback tool [19]. A pressure biofeedback device was used to standardize the abdominal hollowing manoeuvre [12]. The Chattanooga pressure biofeedback device was placed beneath the fifth lumbar vertebra to monitor lumbar movement during performing the abdominal
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N. Tahan et al. / Reliability of the ultrasound measurements of abdominal muscles activity Table 2 The (Mean ± SD) scores for the first and second ultrasound measurements of the TrA during different conditions in each group
Muscle TrA
Measurement
Condition First assessment 3.12 ± 1.04 5.29 ± 1.18
LBP Second assessment 3.08 ± 1 5.47 ± 1.46
Healthy First assessment Second assessment 3.26 ± 0.62 3.05 ± 0.62 5.05 ± 0.99 5.17 ± 1.05
Thickness at rest(mm)
Rest AHM
Maximum thickness(mm)
PFM AHM + PFM
3.78 ± 0.91 5.19 ± 1.2
3.55 ± 0.8 5.51 ± 1.03
3.52 ± 0.78 4.48 ± 0.94
3.3 ± 0.55 5.16 ± 0.98
Thickness change(mm)
AHM PFM AHM + PFM
2.17 ± 1.03 0.66 ± 0.46 2.07 ± 0.62
2.38 ± 0.92 0.47 ± 0.55 2.42 ± 1.09
1.79 ± 0.99 0.26 ± 0.71 1.22 ± 0.75
2.11 ± 1.27 0.24 ± 0.41 2.1 ± 0.99
% thickness change
AHM PFM AHM + PFM
0.77 ± 0.4 1.25 ± 0.23 1.72 ± 0.28
1.82 ± 0.41 1.2 ± 0.28 1.91 ± 0.56
0.59 ± 0.39 1.1 ± 0.26 1.39 ± 0.3
1.7 ± 0.5 1.09 ± 0.15 1.7 ± 0.41
Abbreviations: TrA, Transverse abdominis; OI, Obliqus internus; LBP, Low Back Pain; AHM, Abdominal hollowing manoeuvre; PFM, Pelvic floor muscle; Thickness change, Max thickness – thickness at rest; % thickness change, Thickness change/thickness at rest; ∗ Values in millimeters except % change. Table 3 The (Mean ± SD) scores for the first and second ultrasound measurements of the OI during different conditions in each group Muscle IO
Measurement
Condition First assessment 6.5 ± 1.6 7.8 ± 1.9
LBP Second assessment 6.7 ± 2 8.31 ± 2.44
Healthy First assessment Second assessment 6.28 ± 1.15 6.8 ± 1.7 7.51 ± 0.93 7.7 ± 1.33
Thickness at rest(mm)
Rest AHM
Maximum thickness(mm)
PFM AHM+PFM
7.57 ± 1.48 7.7 ± 1.9
7 ± 1.46 7.74 ± 2.14
6.94 ± 1.2 7.2 ± 0.94
7.05 ± 1.3 6.12 ± 1.22
Thickness change(mm)
AHM PFM AHM+PFM
1.3 ± 0.9 1.04 ± 0.66 1.24 ± 1.3
1.55 ± 1.4 0.24 ± 1.2 0.99 ± 1.6
1.22 ± 0.76 0.65 ± 0. 8 0.92 ± 1
0.88 ± 0.8 0.21 ± 0.86 0.68 ± 1.1
% thickness change
AHM PFM AHM+PFM
0.21 ± 0.15 1.18 ± 0.17 1.21 ± 0.22
1.2 ± 0.25 1.07 ± 0.19 1.18 ± 0.25
0.21 ± 0.16 1.11 ± 0.15 1.17 ± 0.2
1.16 ± 0.17 1.05 ± 0.16 1.1 ± 0.23
Abbreviations: OI, Obliqus internus; LBP, Low Back Pain; AHM, Abdominal hollowing manoeuvre; PFM, Pelvic floor muscle; Thickness change, Max thickness – thickness at rest; % thickness change, Thickness change/thickness at rest; ∗ Values in millimeters except % change.
manoeuvre. The inflatable pillow pressure biofeedback was initially set at 40 mmHg while the subject was at rest. To perform the abdominal hollowing, each participant was instructed to draw their navel up and in towards the spine without moving their upper abdomen or spine, while maintaining a neutral pelvic position to attempt to increase the pressure to 50 mmHg [4,7,12, 29]. To perform PFM contraction, the instruction was given to ‘Draw in and lift the PFM’. All contractions were held for 3 seconds with a rest of 5 seconds between each contraction. The order of contractions was randomly selectedto minimize potential sequence effect. To evaluate the accuracy of pelvic muscle contractions, trans-abdominal ultrasonography was used to investigate the movement of the bladder base during the contraction of pelvic floor muscles [19]. This imaging unit set in B mode (Ultrasonix-ES500, Canada) with a 3.5 MHz curved array transducer.
2.4. Ultrasound measurements The following indices were determined from the all measurements. 1. The resting thickness of TrA and OI muscles. 2. Thickness change of TrA and IO muscles (contracted thickness – resting thickness). 3. Percentage of thickness change of TrA and OI muscles (contracted thickness – resting thickness/resting thickness * 100). 2.5. Data analysis The Kolmogrov-Smirnov test was utilized to assess the normality of distribution for ultrasound measurement of abdominal muscle thickness at the rest, during each condition, thickness change and percentage of thickness change. Based on the previous studies for reliability analyses (Karanicolas 2009; Lexell 2000) the following analyses are used:
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Table 4 Intraclass Correlation Coefficient (ICC(3,1)) values TrA and OI muscles for intra-tester reliability of the ultrasound measurements during different conditions in LBP group Measurement
Condition
TrA ICC3,1 (95% CI) 0.96 0.90 0.84 0.91
SEM (mm∗ ) 0.2 0.3 0.4 0.2
OI ICC3,1 (95% CI) 0.74 0.90 0.84 0.91
SEM (mm∗ ) 0.8 0.6 0.7 0.4
Max thickness
Rest AHM AHM+PFM PFM
Thickness change
AHM AHM+PFM PFM
0.75 0.60 0.76
0.5 0.3 0.2
0.75 0.6 0.76
0.4 0.8 0.3
% thickness change
AHM AHM+PFM PFM
0.79 0.74 0.90
0.1 0.1 0.07
0.79 0.74 0.9
0.06 0.1 0.05
Abbreviations: TrA, Transverse abdominis; OI, Obliqus internus; LBP, Low Back Pain; AHM, Abdominal hollowing manoeuvre; PFM, Pelvic floor muscle; Thickness change, Max thickness – thickness at rest; % thickness change, Thickness change/thickness at rest; *Values in millimeters except % change. Table 5 Intraclass Correlation Coefficient (ICC(3,1)) values TrA and OI muscles for intra-tester reliability of the ultrasound measurements during different conditions in healthy group Measurement
Condition
TrA ICC3,1 (95% CI) 0.8 0.92 0.88 0.87
SEM (mm∗ ) 0.2 0.2 0.01 0.2
OI ICC3,1 (95% CI) 0.77 0.92 0.88 0.87
SEM (mm∗ ) 0.4 0.2 0.3 0.4
Max thickness
Rest AHM AHM+PFM PFM
Thickness change
AHM AHM+PFM PFM
0.86 0.89 0.69
0.3 0.2 0.3
0.86 0.89 0.69
0.2 0.3 0.4
% thickness change
AHM AHM+PF PF
0.86 0.87 0.33
0.1 0.1 0.1
0.86 0.87 0.67
0.05 0.07 0.08
Abbreviations: OI, Obliqus internus; LBP, Low Back Pain; AHM, Abdominal hollowing manoeuvre;PFM, Pelvic floor muscle; Thickness change, Max thickness – thickness at rest; % thickness change, Thickness change/ thickness at rest; *Values in millimeters except % change.
1. Correlational analysis (Intraclass Correlation Coefficient [ICC], two way mixed effects). Correlation or association is greater when ICC value gets closerto 1 [30]. It has been reported that ‘moderate’ association can be judged by ICC values between 0.50 - 0.75and ‘good’ to ‘excellent’ association over 0.75 [31]. 2. Examination of mean changes using Bland Altman plots. Bland Altman plots provide visual demonstration of differences between test and retest measures. Limits of agreement, calculated as the mean difference plus or minus two standard deviations of the differences, as an indicator of error range are also displayed in the Bland Altman plot. Bland Altman plots were drawn only for resting abdominal muscle thickness due to the diversity of conditions.
3. We calculated standard error of measurement (SEM) to make a judgment about the degree that measurements vary for an individual. The SEM is useful in reliability studies to determine the range of scores that would be expected from one assessment session to the next. The standard er√ ror of measurement that was calculated as (SD [1-ICC]).
3. Results The Kolmogrov-Smirnov test showed the normal distribution of all data. Descriptive statistics for the first and second ultrasound measurements of TrA and OI muscles during different conditions in each group are displayed in Tables 2 and 3. A normal pattern of thickness emerged in both groups: IO thickness? TrA thickness. The mean thicknesses of TrA and IO mus-
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cles in AHM and AHM with PFM contraction were larger than resting thicknesses. There was no significant difference in mean thicknesses of TrA and IO muscles during abdominal muscle contraction with and without PFM contraction in both healthy and LBP groups. Tables 4 and 5 presents the ICC (3,1) and SEM values of ultrasound measurements during different conditions in healthy and LBP groups. The results show that the ICCs were excellent for TrA thicknesses in all three conditions in both healthy and LBP. The thickness of TrA muscle in AHM had the highest reliability and was 0.92 and 0.90 in the healthy and LBP group respectively. The ICC of the thickness change and percentage of thickness change ofTrA and IO muscles were lower compared with the thickness at rest in 3 different conditions in both groups. The smallest ICC was the percentage of thickness change of OI in AHM which was 0.47 in healthy group and 0.32 in LBP group (Tables 4, 5). Generally, OI muscle had higher SEM than TrA muscle in the same condition and ranged from 0.01 to 0.4 (in healthy subjects) and 0.05 to 8 (in LBP patients) (Tables 4, 5). Bland Altman plots of TrA and IO muscles thickness measures at rest between test and retest in healthy and LBP individuals demonstrated in Figs 1 (a, b) and 2(a, b). The Bland-Altman plots demonstrated that 95% of the measurements fall between the limits of agreement for test and retest for ultrasound measurement of thickness at rest, for both TrA and OI muscles in both healthy and LBP groups.
4. Discussion This study evaluated the intra- examiner reliability in obtaining ultrasound thickness measurements of the TrA and IO muscles at rest and during different type of contractions during a single session in healthy subjects and patients with LBP. The levels of thickness obtained for TrA and IO muscles in this study are in close agreement with those obtained by B-mode ultrasonography in previous studies [32]. This study shows high intra- examiner reliability for repeat measures of the thickness at rest and during AHM or PFM contraction or combined AHM and PFM contraction of TrA and OI muscles, moderate to excellentreliability for thickness change and percentage of thickness change of TrA and fair to good reliability for thickness change and percentage of thickness change
of OI muscle in both group. These findings are consistent with the previous studies that investigated both in symptomatic [33,34] and asymptomatic [22,25,35] individuals and support our primary hypothesis that UI measurements are adequately reliable in clinical use and research in healthy and patients with LBP. The use of UI in the assessment of the trunk muscles is becoming popular particularly among physiotherapists [22,36,37]. UI has several clinical advantages of being safe, non-invasive and comfortable for patients. It allows real time study of the muscles as they contract and provides direct feedback to the therapists and patient to view the muscle contraction and assist them in the correct muscular activation [38]. This is especially important when the activation pattern of deep muscles such as the deep abdominal muscle is investigated. Change in the thickness of the deep abdominal muscles is measured as an indicator of muscular activity in this method [25,26,36,38]. In this study, we assessed the reliability of ultrasound measurement of the actual deep abdominal muscle thickness at the rest and thickness during performing AHM with and without PFM contraction (voluntary muscle contraction) and during PFM contraction (automatic activity of the antero-lateral abdominal muscles in response to PFM contraction) in both healthy and LBP groups. Similar ICC scores were found in the assessment of voluntary and involuntary activation patterns of the abdominal muscles. Our findings are in agreement with other studies showing good reliability of this method for measuring the abdominal muscle thickness [23, 39]. Norasteh et al. 2007 found good reliability for ultrasonography of the abdominal muscles in asymptomatic subjects and patients with acute LBP. Costa et al. 2009 found excellent reliability values for thickness and moderate reliability values for thickness changes in ultrasound measurements of automatic activation of the lateral abdominal wall muscles using a leg force task in patients with chronic LBP [40]. Reliability can be influenced by several factors such as the participants, therapists and clinical or experimental setting. The procedure of ultrasound measurement has multiple sources of error (e.g. accuracy of measurements of distance between the fascial bands, detection of landmarks, ability to perform the manoeuvres correctly, and position of patient/transducer). The high reliability for measuring the abdominal muscle thickness during AHM or PFM contraction or combined AHM and PFM contraction may be due to the fact that we tried to standardize each contraction and instruct the subjects to perform correct abdomi-
N. Tahan et al. / Reliability of the ultrasound measurements of abdominal muscles activity 2.0
0.5 +1.96 SD 0.23
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3.0
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Fig. 2. The Bland-Altman plot for ultrasound measurements of thickness at rest for OI in LBPand healthysubjects.
nal or PFM contraction using biofeedback tools prior to testing. A pressure biofeedback device was used to standardize AHM [12,41]. We also used transabdominal ultrasound method with a 3.5 MHz curved array transducer to confirm PFM contraction by visualizing the movement of the bladder base. Only contractions with cephalic displacement of bladder base were considered as correct PFM contraction. Another factor is that the image was frozen on the screen and the muscle thickness between the fascial bands was measured by cursor points. The ultrasound transducer was not displaced during the testing procedure as much as possible and the subject’s position was the same for all subjects. In former studies, some researchers have used asymptomatic subjects [22,25,36] while others perform the measurements in patients with LBP [33,34]. Some assessed voluntary and some others assessed automatic activity of abdominal muscles. In this study, we assessed the reliability for both voluntary and automatic activity in healthy subjects and those with LBP. Although this study found high reliability in healthy and LBP groups for both resting thickness measures and maximum thickness change of the TrA and IO muscles, the lower reliability of thickness changes and percentage of thickness change compared with thickness at rest and each condition may be due to the fact that two images (one with the muscle contracted and another with the muscle at rest) are required to determine change in thickness and percentage of thickness change. Therefore, it is not unexpected that estimates of the reliability of percentage of thickness change were consistently lower than those for single thickness measurements and is likely attributable to the fact that change scores are based on imperfect measurements.
The results of current study highlight that B mode UI can provide an objective measure of deep abdominal muscles in different levels of abdominal muscle contraction. This data has usefulness both in a clinical and research framework when investigating deep abdominal muscles function.This might also help to determine the efficacy of prescribed treatments and improvement in chronic LBP patients. 5. Limitation and suggestion for future studies One limitation of this study was assessing only the intra-rater, within-day reliability of UI in different conditions. Further studies need to investigate the interrater and between session reliability of UI measures, especially in functional tasks that evaluate the voluntary and automatic activity of abdominal muscles. 6. Conclusion The results of this study showed high intra-tester reliability for repeat measures of the thickness at rest and thickness during AHM, PFM contraction or AHM with PFM contraction for TrA and OI muscles in healthy and LBP Subjects. Our data demonstrated moderate to substantial reliability for thickness change and percentage of thickness change of TrA muscles in healthy subjects and those with LBP. However, fair to moderate reliability for thickness change and percentage of thickness change of OI muscle was found in both group. Considering good to high reliability for ultrasound measurement of theantero-lateral abdominal muscles, it can be used as a reliable method for assessment of voluntary and automatic activity of the abdominal muscles.
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Acknowledgements This study is based on Nahid Tahan PhD thesis at University of Social Welfare and Rehabilitation Sciences and was approved at student research committee of University of Social Welfare and Rehabilitation Sciences. We would like to acknowledge from all subjects who took part in this study.
[15]
[16]
[17]
[18]
References [19] [1]
[2]
[3]
[4]
[5]
[6]
[7]
[8]
[9] [10]
[11]
[12]
[13]
[14]
Jin K, Sorock GS, Courtney TK. Prevalence of low back pain in three occupational groups in Shanghai, People’s Republic of China. Journal of Safety Research. 2004; 35(1): 23-8. Hodges P, Richardson C. Inefficient muscular stabilization of the lumbar spine associated with low back pain. A motor control evaluation of transversus abdominis. Spine. 1996; 21: 2640-50. Hodges PW, Richardson CA. Delayed postural contraction of transversus abdominis in low back pain associated with movement of the lower limb. Journal of Spinal Disorders and Techniques. 1998; 11(1): 46. Jull GA, Richardson CA. Motor control problems in patients with spinal pain: A new direction for therapeutic exercise. Journal of Manipulative and Physiological Therapeutics. 2000; 23(2): 115-7. Cholewicki J, McGill S. Mechanical stability of the in vivo lumbar spine: implications for injury and chronic low back pain. Clinical Biomechanics. 1996; 11(1): 1-15. Bergmark A. Stability of the lumbar spine. A study in mechanical engineering. Acta Orthopaedica Scandinavica Supplementum. 1989; 230: 1. Richardson C, Jull G, Hodges P, Hides J. Therapeutic exercise for spinal segmental stabilization in low back pain: scientific basis and clinical approach: Churchill Livingstone, 1999. Jull G, Richardson C. Rehabilitation of active stabilization of the lumbar spine. Physical Therapy of the Lumbar Spine 2nd de Churchill Livingstone, 1994. Slosberg M. Core Stabilization Strategies: Abdominal Hollowing vs. Bracing. Dynamic Chiropractic 2009; 27(21). Sparkes V, Lambert C, Keith A, Rees D, Terry G. Spinal stability exercises: evidence of preferential activation of internal oblique muscles in 3 and 2 point kneeling exercises. Physical Therapy in Sport. 2006; 7(4): 174-5. Vera-Garcia FJ, Elvira JLL, Brown SHM, McGill SM. Effects of abdominal stabilization maneuvers on the control of spine motion and stability against sudden trunk perturbations. Journal of Electromyography and Kinesiology. 2007; 17(5): 55667. Allison G, Godfrey P, Robinson G. EMG signal amplitude assessment during abdominal bracing and hollowing. Journal of Electromyography and Kinesiology. 1998; 8(1): 51-7. Bø K, Stien R. Needle EMG registration of striated urethral wall and pelvic floor muscle activity patterns during cough, Valsalva, abdominal, hip adductor, and gluteal muscle contractions in nulliparous healthy females. Neurourology and Urodynamics. 1994; 13(1): 35-41. Sapsford R, Hodges P, Richardson C, Cooper D, Markwell S, Jull G. Co activation of the abdominal and pelvic floor muscles during voluntary exercises. Neurourology and Urodynamics. 2001; 20(1): 31-42.
[20]
[21]
[22]
[23]
[24]
[25]
[26]
[27]
[28]
[29]
[30] [31]
[32]
Hodges PW, Eriksson AEM, Shirley D, SC G. Intraabdominal pressure increases stiffness of the lumbar spine. Journal of Biomechanics. 2005; 38: 1873-80. Sapsford R, Hodges P, Richardson C, Cooper D, S.J. Markwell S, JA J. Co-activation of the Abdominal and Pelvic Floor Muscles During Voluntary Exercises Neurourology and Urodynamics. 2001(20): 31-42. Sapsford RR, Hodges PW. Contraction of the pelvic floor muscles during abdominal maneuvers* 1. Archives of physical medicine and rehabilitation. 2001; 82(8): 1081-8. Neumann P, Gill V. Pelvic floor and abdominal muscle interaction: EMG activity and intra-abdominal pressure. International Urogynecology Journal. 2002; 13(2): 125-32. Arab AM, Behbahani RB, Lorestani L, Azari A. Assessment of pelvic floor muscle function in women with and without low back pain using transabdominal ultrasound. Manual therapy. 2010; 15(3): 235-9. Stokes M, Young A. Measurement of Quadriceps Cross– sectional Area by Ultrasonography: A Description of the Technique and its Applications in Physiotherapy. Informa Healthcare; 1986, pp. 31-6. Hodges P, Pengel L, Herbert R, Gandevia S. Measurement of muscle contraction with ultrasound imaging. Muscle and Nerve. 2003; 27(6): 682-92. McMeeken J, Beith I, Newham D, Milligan P, Critchley D. The relationship between EMG and change in thickness of transversus abdominis. Clinical Biomechanics. 2004; 19(4): 337-42. Costa LO, Maher CG, Latimer J, Hodges PW, D S. An investigation of the reproducibility of ultrasound measures of abdominal muscle activation in patients with chronic nonspecific low back pain. Eur Spine J. 2009; 18: 1059-65. Nourbakhsh MR, Arab AM. Relationship between mechanical factors and incidence of low back pain. The Journal of Orthopaedic and Sports Physical Therapy. 2002; 32(9): 447. Ainscough-Potts AM, Morrissey MC, Critchley D. The response of the transverse abdominis and internal oblique muscles to different postures. Manual Therapy. 2006; 11(1): 5460. Critchley D. Instructing pelvic floor contraction facilitates transversus abdominis thickness increase during low abdominal hollowing. Physiotherapy Research International. 2002; 7(2): 65-75. Ferreira PH, Ferreira ML, Hodges PW. Changes in recruitment of the abdominal muscles in people with low back pain: ultrasound measurement of muscle activity. Spine. 2004; 29(22): 2560. Teyhen DS, Gill NW, Whittaker JL, Henry SM, Hides JA, Hodges P. Rehabilitative ultrasound imaging of the abdominal muscles. The Journal of Orthopaedic and Sports Physical Therapy. 2007; 37(8): 450. Beith I, Synnott R, Newman S. Abdominal muscle activity during the abdominal hollowing manoeuvre in the four point kneeling and prone positions. Manual Therapy. 2001; 6(2): 82-7. Watkins MP, Library R. Foundations of clinical research: applications to practice: Pearson/Prentice Hall, 2009. Rankin G, Stokes M. Reliability of assessment tools in rehabilitation: an illustration of appropriate statistical analyses. Clinical Rehabilitation. 1998; 12(3): 187-99. Mannion AF, Pulkovski N, Gubler D, Gorelick M, O’Riordan D, Loupas T, et al. Muscle thickness changes during abdominal hollowing: An assessment of between-day measurement
N. Tahan et al. / Reliability of the ultrasound measurements of abdominal muscles activity
[33]
[34]
[35]
[36]
[37]
error in controls and patients with chronic low back pain. European Spine Journal. 2008; 17(4): 494-501. Critchley DJ, Coutts FJ. Abdominal Muscle Function in Chronic Low Back Pain Patients: Measurement with real-time ultrasound scanning. Physiotherapy. 2002; 88(6): 322-32. Teyhen DS, .Miltenberger CE, Delters HM, Deltoro YM, Pulliam JN, Childs J, et al. The use of ultrasound imaging of the abdominal drawing-in maneuver in subjects with low back pain. The Journal of Orthopaedic and Sports Physical Therapy. 2005; 35(6): 346-55. Bunce S, Moore A, Hough A. M-mode ultrasound: A reliable measure of transversus abdominis thickness? Clinical Biomechanics. 2002; 17(4): 315-7. Bunce S, Moore A, Hough A. M-mode ultrasound: A reliable measure of transversus abdominis thickness? Clin Biomech (Bristol, Avon). 2002; 17: 315-7. Hodges PW, Pengel LHM, Herbert RD, Gandevia SC. Measurement of muscle contraction with ultrasound imaging.
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Wiley Online Library; 2003, pp. 682-92. Henry SM, Westervelt KC. The use of real-time ultrasound feedback in teaching abdominal hollowing exercises to healthy subjects. The Journal of Orthopaedic and Sports Physical Therapy. 2005; 35(6): 338-45. [39] Norasteh A, Ebrahimi E, Salavati M, Rafiei J, Abbasnejad E. Reliability of B-mode ultrasonography for abdominal muscles in asymptomatic and patients with acute low back pain. Journal of Bodywork and Movement Therapies. 2007; 11(1): 17-20. [40] Costa LOP, Maher CG, Latimer J, Smeets RJEM. Reproducibility of rehabilitative ultrasound imaging for the measurement of abdominal muscle activity: A systematic review. Physical therapy. 2009; 89(8): 756. [41] Cairns MC, Harrison K, Wright C. Pressure Biofeedback: A useful tool in the quantification of abdominal muscular dysfunction? Physiotherapy. 2000; 86(3): 127-38. [38]
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Journal of Back and Musculoskeletal Rehabilitation 27 (2014) 339–347 DOI 10.3233/BMR-130453 IOS Press
Reliability of the ultrasound measurements of abdominal muscles activity when activated with and without pelvic floor muscles contraction Nahid Tahana,∗, Omid Rasoulib , Amir Massoud Arabc , Khosro Khademia and Elham Neisani Samanid a Department of Physical Therapy, Faculty of Rehabilitation Science, Shahid Beheshti University of Medical Sciences, Tehran, Iran b Department of Physical Therapy, Faculty of Health Education and Social Work, Sør-Trøndelag University College (HiST), Trondheim, Norway c Department of Physical Therapy, University of Social Welfare and Rehabilitation Sciences, Evin, Tehran, Iran d Taleghani Hospital, Shahid Beheshti University of Medical Sciences, Tehran, Iran
Abstract. BACKGROUND: Synergistic co-activation of the abdominal and pelvic floor muscles (PFM) has been shown in literature. Some studies have assessed the reliability of ultrasound measures of the abdominal muscles. OBJECTIVE: The aim of this study was to determine the reliability of ultrasound measurements of transverses abdominis (TrA) and obliquus internus (OI) muscles during different conditions (PFM contraction, abdominal hollowing manoeuvre (AHM) with and without PFM contraction) in participants with and without chronic low back pain (LBP). METHODS: 21 participants (9 with LBP, 12 healthy) participated in the study. The reliability of thickness measurements at rest and during each condition and thickness changes and percentage of this changes at different conditions were assessed. RESULTS: The results showed high reliability of the thickness measurement at rest and during each condition of TrA and OI muscles, moderate to substantial reliability for the thickness change and percentage of thickness change of TrA, and fair to moderate reliability of the thickness change and percentage of thickness change of OI in both groups. CONCLUSIONS: Ultrasound imaging can be used as a reliable method for assessment of abdominal muscle activity with and without PFM contraction. Keywords: Low back pain, pelvic floor muscles, abdominal muscles, reliability
1. Introduction Low back pain (LBP) is one of the most frequent complaints in today’s societies. Previous studies have indicated that 70–80% of the western population have had at least one episode of LBP in their lifetime [1]. ∗ Corresponding author: Dr. Nahid Tahan, Damavand Ave, Emam Hossein Square, P.O Box 1616913111, Tehran, Iran. Tel.: +98 21 77548496; Fax: +98 21 77561406; E-mail: nahidta2431@Gmail. com.
Several factors, based on clinical findings and scientific experiments, have been associated with the development of LBP. However, during the recent decades the main focus has been placed on segmental lumbar spine instability and its association with LBP. There is substantial evidence indicating that main impairment in patients with chronic LBP is deep local muscles dysfunction [2–4], which may affects spinal stability [5]. The deep antero-lateral abdominal muscles including transverse abdominis (TrA) and obliqus internus (OI) play an important role in providing spinal stability
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during functional activities [6,7]. Accordingly, during the past decade the main focus of rehabilitation program for patients with LBP has been placed on specific therapeutic exercises for key stabilizing muscles including deep abdominal muscles [8]. The abdominal hollowing maneuver (AHM) is commonly used to assess and rehabilitate the abdominal muscles [9–11]. The abdominal hollowing manoeuvre is performed to activate deep antero-lateral abdominal muscles [8]. This is achieved by instructing the participants to hollow their abdomen by drawing their navel up and in towards the spine [12]. Recent studies have led to understanding of the synergistic co-activation between the abdominal and pelvic floor muscles (PFM) for development of intraabdominal pressure and load transfer [13–15]. Electromyographic (EMG)studies have demonstrated that all the abdominal muscles are activated during voluntary contraction of the PFM [16,17]. However, normalized EMG activity was greater for OI and TrA than obliqus externus (OE) [18]. Accordingly, the PFM are generally accepted as a part of the trunk stability mechanism. PFM dysfunction has been reported in individuals with LBP compared with healthy subjects [19]. Ultrasound is a safe, cost-effective and accessible method for visualizing and measuring the deep muscles in real time manner [20], that allows direct visualisation of the abdominal muscles and can measure the change in thickness of a muscle as it contracts over the time. A variety of measurement tools have been used by physical therapists to assess the abdominal muscle functions in subjects with LBP attending physical therapy clinics. More recently, there is more interest in the use of real-time ultrasound imaging as valid method to evaluate muscle structure, function and activation patterns. The ultrasound imaging (UI) allows direct visualization for real time study of the muscles as they contract over the time. This is especially important when the deep abdominal muscle activity is investigated. Changes in the thickness of abdominal muscles are measured as an indicator of abdominal muscle activity during ultrasound imaging [21]. Validity studies have compared ultrasound measurements with EMG and found good to high correlation between measurements of muscle thickness and EMG activity at low activity levels [21,22]. However, these researchers found that OE behaved in a different way from TrA and OI and there was no consistent relationship between muscle thickness and EMG activity of OE. The reliability of this method for measuring changes in TrA mus-
Table 1 Demographic data for the Healthy and LBP groups Variables Age (year)
Group Healthy LBP
Mean ± SD 24.9 ± 3.8 26.5 ± 8.5
Minimum 21.00 18.00
Maximum 33.00 47.00
Weight (kg)
Healthy LBP
61.00 ± 10.4 61.3 ± 9.5
45.00 48.00
76.00 77.00
Height (cm)
Healthy LBP
160 ± 10 160 ± 5
150 155
183 171
22.1 ± 3.09 22.7 ± 2.2
18.7 19.9
28.5 26.6
BMI (Kg/m2 ) Healthy LBP
cle thickness has been assessed previously. Costa reported moderate reliability for thickness changes [23]. These findings support using of ultrasound imaging as a non-invasive technique to measure TrA and OI muscle thickness and estimate relative muscle activity when these muscles are voluntarily contracted. Although several studies have investigated the reliability of ultrasound measures of the abdominal muscles, most have investigated reliability during resting states or when the abdominal muscles contracted alone. To our knowledge, no study has directly investigated the reliability of ultrasound measurement of the abdominal muscle activity during contraction with and without PFM contraction so the purpose of this study was to evaluate the intra-examiner reliability of the ultrasound measurements of TrA and OI muscles at rest, during PFM contraction and during abdominal hollowing manoeuvre with and without PFM contraction in subjects with and without non-specific chronic LBP.
2. Materials and methods 2.1. Participants A total of 21 participants (9 with LBP, 12 healthy individuals) participated in the study. The subject population in this study was a sample of convenience made up of subjects who were between the ages of 18 and 47 years. Participants with LBP were selected among the patients visited in the orthopedic and physical therapy clinics. All the participants in the study filled out a simple health questionnaire. Those who met the selection criteria were included in the study. All the participants signed an informed consent form approved by the human ethics committee of university of Social Welfare and Rehabilitation Sciences. The demographic data of the participants are shown in Table 1.
N. Tahan et al. / Reliability of the ultrasound measurements of abdominal muscles activity 2.0
2.0
+1.96 SD 1.42
1.5 1.0
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4.0
4.5
0
1
(a) LBP subjects
2 3 AVERAGE of Test and Re-test
4
5
(b) Healthy Subjects
Fig. 1. The Bland-Altman plot for ultrasound measurements of thickness at rest for TrA in LBPand healthy subjects.
Patients were included if they had a history of LBP for more than six weeks before the study or had on and off back pain and had experienced at least three episodes of LBP, each lasting more than one week, during the year before the study [24]. A visual analogue scale (VAS) was used to assess the pain intensity. VAS score of 2 or less on the day of test was considered as a further inclusion criterion. Healthy participants had no complaint of any pain or dysfunction in their low back, pelvis, thoracic and lower extremities. Participants were excluded if they had a history of surgery in the lumbar spine, radiculopathy, persistent severe pain, neurological symptoms, severe spinal instability, osteoporosis, structural deformity, systemic inflammatory disease, previous spinal fusion, severe cardiovascular diseases, acute infection, recent abdominal surgery and uncontrolled alcohol/drug abuse. A further exclusion criterion was pregnancy. 2.2. Ultrasound imaging A diagnostic ultrasound imaging unit set in B-mode (Ultrasonix-ES500, Canada) with a linear array transducer (7.5 MHz) was used to measure the abdominal muscle thickness at rest, during PFM contraction and during abdominal hollowing manoeuvre with and without PFM contraction based on the method explained by others [22,25–28]. The measurements were made on the right side of the abdominal wall. The participants were tested in crook-lying position with one pillow underneath the head and knees. The lumbar spine was positioned in neutral. The skinwas marked to confirm the exact po-
sition of the transducer on the abdominal wall. The transducer was transversely located across the abdominal wall, 25 mm antero-medial to the midway point between the 12th rib and the iliac crestover the anterior axillary line to obtain a clear image of the deep abdominal layers [22]. The ultrasound transducer was not displaced during the testing procedure. Actual muscle thicknesses (TrA, OI) at rest (end of expiration) and during contractions (PFM contraction, abdominal hollowing manoeuvre with and without PFM contraction) were measured. The cursor points carefully measured the muscle thickness between the inside edge of fascial bands in millimetres (mm) (Fig. 1). The maximum thicknesses at rest and during each contraction for the abdominal muscles (TrA, OI) were calculated. 2.3. Procedures The participants were assessed two times for intratester reliability of the ultrasound measurements. For this purpose, at first the examiner performed the measurements in participants, and then repeated the measurements after 30 minutes in a blinded fashion and random order with the same procedure. The participants were allowed to get up, walk around and be active during 30 minutes rest. Prior to testing, participants were trained by a physiotherapist to perform the abdominal and PFM contractions correctly using ultrasound as a biofeedback tool [19]. A pressure biofeedback device was used to standardize the abdominal hollowing manoeuvre [12]. The Chattanooga pressure biofeedback device was placed beneath the fifth lumbar vertebra to monitor lumbar movement during performing the abdominal
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N. Tahan et al. / Reliability of the ultrasound measurements of abdominal muscles activity Table 2 The (Mean ± SD) scores for the first and second ultrasound measurements of the TrA during different conditions in each group
Muscle TrA
Measurement
Condition First assessment 3.12 ± 1.04 5.29 ± 1.18
LBP Second assessment 3.08 ± 1 5.47 ± 1.46
Healthy First assessment Second assessment 3.26 ± 0.62 3.05 ± 0.62 5.05 ± 0.99 5.17 ± 1.05
Thickness at rest(mm)
Rest AHM
Maximum thickness(mm)
PFM AHM + PFM
3.78 ± 0.91 5.19 ± 1.2
3.55 ± 0.8 5.51 ± 1.03
3.52 ± 0.78 4.48 ± 0.94
3.3 ± 0.55 5.16 ± 0.98
Thickness change(mm)
AHM PFM AHM + PFM
2.17 ± 1.03 0.66 ± 0.46 2.07 ± 0.62
2.38 ± 0.92 0.47 ± 0.55 2.42 ± 1.09
1.79 ± 0.99 0.26 ± 0.71 1.22 ± 0.75
2.11 ± 1.27 0.24 ± 0.41 2.1 ± 0.99
% thickness change
AHM PFM AHM + PFM
0.77 ± 0.4 1.25 ± 0.23 1.72 ± 0.28
1.82 ± 0.41 1.2 ± 0.28 1.91 ± 0.56
0.59 ± 0.39 1.1 ± 0.26 1.39 ± 0.3
1.7 ± 0.5 1.09 ± 0.15 1.7 ± 0.41
Abbreviations: TrA, Transverse abdominis; OI, Obliqus internus; LBP, Low Back Pain; AHM, Abdominal hollowing manoeuvre; PFM, Pelvic floor muscle; Thickness change, Max thickness – thickness at rest; % thickness change, Thickness change/thickness at rest; ∗ Values in millimeters except % change. Table 3 The (Mean ± SD) scores for the first and second ultrasound measurements of the OI during different conditions in each group Muscle IO
Measurement
Condition First assessment 6.5 ± 1.6 7.8 ± 1.9
LBP Second assessment 6.7 ± 2 8.31 ± 2.44
Healthy First assessment Second assessment 6.28 ± 1.15 6.8 ± 1.7 7.51 ± 0.93 7.7 ± 1.33
Thickness at rest(mm)
Rest AHM
Maximum thickness(mm)
PFM AHM+PFM
7.57 ± 1.48 7.7 ± 1.9
7 ± 1.46 7.74 ± 2.14
6.94 ± 1.2 7.2 ± 0.94
7.05 ± 1.3 6.12 ± 1.22
Thickness change(mm)
AHM PFM AHM+PFM
1.3 ± 0.9 1.04 ± 0.66 1.24 ± 1.3
1.55 ± 1.4 0.24 ± 1.2 0.99 ± 1.6
1.22 ± 0.76 0.65 ± 0. 8 0.92 ± 1
0.88 ± 0.8 0.21 ± 0.86 0.68 ± 1.1
% thickness change
AHM PFM AHM+PFM
0.21 ± 0.15 1.18 ± 0.17 1.21 ± 0.22
1.2 ± 0.25 1.07 ± 0.19 1.18 ± 0.25
0.21 ± 0.16 1.11 ± 0.15 1.17 ± 0.2
1.16 ± 0.17 1.05 ± 0.16 1.1 ± 0.23
Abbreviations: OI, Obliqus internus; LBP, Low Back Pain; AHM, Abdominal hollowing manoeuvre; PFM, Pelvic floor muscle; Thickness change, Max thickness – thickness at rest; % thickness change, Thickness change/thickness at rest; ∗ Values in millimeters except % change.
manoeuvre. The inflatable pillow pressure biofeedback was initially set at 40 mmHg while the subject was at rest. To perform the abdominal hollowing, each participant was instructed to draw their navel up and in towards the spine without moving their upper abdomen or spine, while maintaining a neutral pelvic position to attempt to increase the pressure to 50 mmHg [4,7,12, 29]. To perform PFM contraction, the instruction was given to ‘Draw in and lift the PFM’. All contractions were held for 3 seconds with a rest of 5 seconds between each contraction. The order of contractions was randomly selectedto minimize potential sequence effect. To evaluate the accuracy of pelvic muscle contractions, trans-abdominal ultrasonography was used to investigate the movement of the bladder base during the contraction of pelvic floor muscles [19]. This imaging unit set in B mode (Ultrasonix-ES500, Canada) with a 3.5 MHz curved array transducer.
2.4. Ultrasound measurements The following indices were determined from the all measurements. 1. The resting thickness of TrA and OI muscles. 2. Thickness change of TrA and IO muscles (contracted thickness – resting thickness). 3. Percentage of thickness change of TrA and OI muscles (contracted thickness – resting thickness/resting thickness * 100). 2.5. Data analysis The Kolmogrov-Smirnov test was utilized to assess the normality of distribution for ultrasound measurement of abdominal muscle thickness at the rest, during each condition, thickness change and percentage of thickness change. Based on the previous studies for reliability analyses (Karanicolas 2009; Lexell 2000) the following analyses are used:
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Table 4 Intraclass Correlation Coefficient (ICC(3,1)) values TrA and OI muscles for intra-tester reliability of the ultrasound measurements during different conditions in LBP group Measurement
Condition
TrA ICC3,1 (95% CI) 0.96 0.90 0.84 0.91
SEM (mm∗ ) 0.2 0.3 0.4 0.2
OI ICC3,1 (95% CI) 0.74 0.90 0.84 0.91
SEM (mm∗ ) 0.8 0.6 0.7 0.4
Max thickness
Rest AHM AHM+PFM PFM
Thickness change
AHM AHM+PFM PFM
0.75 0.60 0.76
0.5 0.3 0.2
0.75 0.6 0.76
0.4 0.8 0.3
% thickness change
AHM AHM+PFM PFM
0.79 0.74 0.90
0.1 0.1 0.07
0.79 0.74 0.9
0.06 0.1 0.05
Abbreviations: TrA, Transverse abdominis; OI, Obliqus internus; LBP, Low Back Pain; AHM, Abdominal hollowing manoeuvre; PFM, Pelvic floor muscle; Thickness change, Max thickness – thickness at rest; % thickness change, Thickness change/thickness at rest; *Values in millimeters except % change. Table 5 Intraclass Correlation Coefficient (ICC(3,1)) values TrA and OI muscles for intra-tester reliability of the ultrasound measurements during different conditions in healthy group Measurement
Condition
TrA ICC3,1 (95% CI) 0.8 0.92 0.88 0.87
SEM (mm∗ ) 0.2 0.2 0.01 0.2
OI ICC3,1 (95% CI) 0.77 0.92 0.88 0.87
SEM (mm∗ ) 0.4 0.2 0.3 0.4
Max thickness
Rest AHM AHM+PFM PFM
Thickness change
AHM AHM+PFM PFM
0.86 0.89 0.69
0.3 0.2 0.3
0.86 0.89 0.69
0.2 0.3 0.4
% thickness change
AHM AHM+PF PF
0.86 0.87 0.33
0.1 0.1 0.1
0.86 0.87 0.67
0.05 0.07 0.08
Abbreviations: OI, Obliqus internus; LBP, Low Back Pain; AHM, Abdominal hollowing manoeuvre;PFM, Pelvic floor muscle; Thickness change, Max thickness – thickness at rest; % thickness change, Thickness change/ thickness at rest; *Values in millimeters except % change.
1. Correlational analysis (Intraclass Correlation Coefficient [ICC], two way mixed effects). Correlation or association is greater when ICC value gets closerto 1 [30]. It has been reported that ‘moderate’ association can be judged by ICC values between 0.50 - 0.75and ‘good’ to ‘excellent’ association over 0.75 [31]. 2. Examination of mean changes using Bland Altman plots. Bland Altman plots provide visual demonstration of differences between test and retest measures. Limits of agreement, calculated as the mean difference plus or minus two standard deviations of the differences, as an indicator of error range are also displayed in the Bland Altman plot. Bland Altman plots were drawn only for resting abdominal muscle thickness due to the diversity of conditions.
3. We calculated standard error of measurement (SEM) to make a judgment about the degree that measurements vary for an individual. The SEM is useful in reliability studies to determine the range of scores that would be expected from one assessment session to the next. The standard er√ ror of measurement that was calculated as (SD [1-ICC]).
3. Results The Kolmogrov-Smirnov test showed the normal distribution of all data. Descriptive statistics for the first and second ultrasound measurements of TrA and OI muscles during different conditions in each group are displayed in Tables 2 and 3. A normal pattern of thickness emerged in both groups: IO thickness? TrA thickness. The mean thicknesses of TrA and IO mus-
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cles in AHM and AHM with PFM contraction were larger than resting thicknesses. There was no significant difference in mean thicknesses of TrA and IO muscles during abdominal muscle contraction with and without PFM contraction in both healthy and LBP groups. Tables 4 and 5 presents the ICC (3,1) and SEM values of ultrasound measurements during different conditions in healthy and LBP groups. The results show that the ICCs were excellent for TrA thicknesses in all three conditions in both healthy and LBP. The thickness of TrA muscle in AHM had the highest reliability and was 0.92 and 0.90 in the healthy and LBP group respectively. The ICC of the thickness change and percentage of thickness change ofTrA and IO muscles were lower compared with the thickness at rest in 3 different conditions in both groups. The smallest ICC was the percentage of thickness change of OI in AHM which was 0.47 in healthy group and 0.32 in LBP group (Tables 4, 5). Generally, OI muscle had higher SEM than TrA muscle in the same condition and ranged from 0.01 to 0.4 (in healthy subjects) and 0.05 to 8 (in LBP patients) (Tables 4, 5). Bland Altman plots of TrA and IO muscles thickness measures at rest between test and retest in healthy and LBP individuals demonstrated in Figs 1 (a, b) and 2(a, b). The Bland-Altman plots demonstrated that 95% of the measurements fall between the limits of agreement for test and retest for ultrasound measurement of thickness at rest, for both TrA and OI muscles in both healthy and LBP groups.
4. Discussion This study evaluated the intra- examiner reliability in obtaining ultrasound thickness measurements of the TrA and IO muscles at rest and during different type of contractions during a single session in healthy subjects and patients with LBP. The levels of thickness obtained for TrA and IO muscles in this study are in close agreement with those obtained by B-mode ultrasonography in previous studies [32]. This study shows high intra- examiner reliability for repeat measures of the thickness at rest and during AHM or PFM contraction or combined AHM and PFM contraction of TrA and OI muscles, moderate to excellentreliability for thickness change and percentage of thickness change of TrA and fair to good reliability for thickness change and percentage of thickness change
of OI muscle in both group. These findings are consistent with the previous studies that investigated both in symptomatic [33,34] and asymptomatic [22,25,35] individuals and support our primary hypothesis that UI measurements are adequately reliable in clinical use and research in healthy and patients with LBP. The use of UI in the assessment of the trunk muscles is becoming popular particularly among physiotherapists [22,36,37]. UI has several clinical advantages of being safe, non-invasive and comfortable for patients. It allows real time study of the muscles as they contract and provides direct feedback to the therapists and patient to view the muscle contraction and assist them in the correct muscular activation [38]. This is especially important when the activation pattern of deep muscles such as the deep abdominal muscle is investigated. Change in the thickness of the deep abdominal muscles is measured as an indicator of muscular activity in this method [25,26,36,38]. In this study, we assessed the reliability of ultrasound measurement of the actual deep abdominal muscle thickness at the rest and thickness during performing AHM with and without PFM contraction (voluntary muscle contraction) and during PFM contraction (automatic activity of the antero-lateral abdominal muscles in response to PFM contraction) in both healthy and LBP groups. Similar ICC scores were found in the assessment of voluntary and involuntary activation patterns of the abdominal muscles. Our findings are in agreement with other studies showing good reliability of this method for measuring the abdominal muscle thickness [23, 39]. Norasteh et al. 2007 found good reliability for ultrasonography of the abdominal muscles in asymptomatic subjects and patients with acute LBP. Costa et al. 2009 found excellent reliability values for thickness and moderate reliability values for thickness changes in ultrasound measurements of automatic activation of the lateral abdominal wall muscles using a leg force task in patients with chronic LBP [40]. Reliability can be influenced by several factors such as the participants, therapists and clinical or experimental setting. The procedure of ultrasound measurement has multiple sources of error (e.g. accuracy of measurements of distance between the fascial bands, detection of landmarks, ability to perform the manoeuvres correctly, and position of patient/transducer). The high reliability for measuring the abdominal muscle thickness during AHM or PFM contraction or combined AHM and PFM contraction may be due to the fact that we tried to standardize each contraction and instruct the subjects to perform correct abdomi-
N. Tahan et al. / Reliability of the ultrasound measurements of abdominal muscles activity 2.0
0.5 +1.96 SD 0.23
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Fig. 2. The Bland-Altman plot for ultrasound measurements of thickness at rest for OI in LBPand healthysubjects.
nal or PFM contraction using biofeedback tools prior to testing. A pressure biofeedback device was used to standardize AHM [12,41]. We also used transabdominal ultrasound method with a 3.5 MHz curved array transducer to confirm PFM contraction by visualizing the movement of the bladder base. Only contractions with cephalic displacement of bladder base were considered as correct PFM contraction. Another factor is that the image was frozen on the screen and the muscle thickness between the fascial bands was measured by cursor points. The ultrasound transducer was not displaced during the testing procedure as much as possible and the subject’s position was the same for all subjects. In former studies, some researchers have used asymptomatic subjects [22,25,36] while others perform the measurements in patients with LBP [33,34]. Some assessed voluntary and some others assessed automatic activity of abdominal muscles. In this study, we assessed the reliability for both voluntary and automatic activity in healthy subjects and those with LBP. Although this study found high reliability in healthy and LBP groups for both resting thickness measures and maximum thickness change of the TrA and IO muscles, the lower reliability of thickness changes and percentage of thickness change compared with thickness at rest and each condition may be due to the fact that two images (one with the muscle contracted and another with the muscle at rest) are required to determine change in thickness and percentage of thickness change. Therefore, it is not unexpected that estimates of the reliability of percentage of thickness change were consistently lower than those for single thickness measurements and is likely attributable to the fact that change scores are based on imperfect measurements.
The results of current study highlight that B mode UI can provide an objective measure of deep abdominal muscles in different levels of abdominal muscle contraction. This data has usefulness both in a clinical and research framework when investigating deep abdominal muscles function.This might also help to determine the efficacy of prescribed treatments and improvement in chronic LBP patients. 5. Limitation and suggestion for future studies One limitation of this study was assessing only the intra-rater, within-day reliability of UI in different conditions. Further studies need to investigate the interrater and between session reliability of UI measures, especially in functional tasks that evaluate the voluntary and automatic activity of abdominal muscles. 6. Conclusion The results of this study showed high intra-tester reliability for repeat measures of the thickness at rest and thickness during AHM, PFM contraction or AHM with PFM contraction for TrA and OI muscles in healthy and LBP Subjects. Our data demonstrated moderate to substantial reliability for thickness change and percentage of thickness change of TrA muscles in healthy subjects and those with LBP. However, fair to moderate reliability for thickness change and percentage of thickness change of OI muscle was found in both group. Considering good to high reliability for ultrasound measurement of theantero-lateral abdominal muscles, it can be used as a reliable method for assessment of voluntary and automatic activity of the abdominal muscles.
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N. Tahan et al. / Reliability of the ultrasound measurements of abdominal muscles activity
Acknowledgements This study is based on Nahid Tahan PhD thesis at University of Social Welfare and Rehabilitation Sciences and was approved at student research committee of University of Social Welfare and Rehabilitation Sciences. We would like to acknowledge from all subjects who took part in this study.
[15]
[16]
[17]
[18]
References [19] [1]
[2]
[3]
[4]
[5]
[6]
[7]
[8]
[9] [10]
[11]
[12]
[13]
[14]
Jin K, Sorock GS, Courtney TK. Prevalence of low back pain in three occupational groups in Shanghai, People’s Republic of China. Journal of Safety Research. 2004; 35(1): 23-8. Hodges P, Richardson C. Inefficient muscular stabilization of the lumbar spine associated with low back pain. A motor control evaluation of transversus abdominis. Spine. 1996; 21: 2640-50. Hodges PW, Richardson CA. Delayed postural contraction of transversus abdominis in low back pain associated with movement of the lower limb. Journal of Spinal Disorders and Techniques. 1998; 11(1): 46. Jull GA, Richardson CA. Motor control problems in patients with spinal pain: A new direction for therapeutic exercise. Journal of Manipulative and Physiological Therapeutics. 2000; 23(2): 115-7. Cholewicki J, McGill S. Mechanical stability of the in vivo lumbar spine: implications for injury and chronic low back pain. Clinical Biomechanics. 1996; 11(1): 1-15. Bergmark A. Stability of the lumbar spine. A study in mechanical engineering. Acta Orthopaedica Scandinavica Supplementum. 1989; 230: 1. Richardson C, Jull G, Hodges P, Hides J. Therapeutic exercise for spinal segmental stabilization in low back pain: scientific basis and clinical approach: Churchill Livingstone, 1999. Jull G, Richardson C. Rehabilitation of active stabilization of the lumbar spine. Physical Therapy of the Lumbar Spine 2nd de Churchill Livingstone, 1994. Slosberg M. Core Stabilization Strategies: Abdominal Hollowing vs. Bracing. Dynamic Chiropractic 2009; 27(21). Sparkes V, Lambert C, Keith A, Rees D, Terry G. Spinal stability exercises: evidence of preferential activation of internal oblique muscles in 3 and 2 point kneeling exercises. Physical Therapy in Sport. 2006; 7(4): 174-5. Vera-Garcia FJ, Elvira JLL, Brown SHM, McGill SM. Effects of abdominal stabilization maneuvers on the control of spine motion and stability against sudden trunk perturbations. Journal of Electromyography and Kinesiology. 2007; 17(5): 55667. Allison G, Godfrey P, Robinson G. EMG signal amplitude assessment during abdominal bracing and hollowing. Journal of Electromyography and Kinesiology. 1998; 8(1): 51-7. Bø K, Stien R. Needle EMG registration of striated urethral wall and pelvic floor muscle activity patterns during cough, Valsalva, abdominal, hip adductor, and gluteal muscle contractions in nulliparous healthy females. Neurourology and Urodynamics. 1994; 13(1): 35-41. Sapsford R, Hodges P, Richardson C, Cooper D, Markwell S, Jull G. Co activation of the abdominal and pelvic floor muscles during voluntary exercises. Neurourology and Urodynamics. 2001; 20(1): 31-42.
[20]
[21]
[22]
[23]
[24]
[25]
[26]
[27]
[28]
[29]
[30] [31]
[32]
Hodges PW, Eriksson AEM, Shirley D, SC G. Intraabdominal pressure increases stiffness of the lumbar spine. Journal of Biomechanics. 2005; 38: 1873-80. Sapsford R, Hodges P, Richardson C, Cooper D, S.J. Markwell S, JA J. Co-activation of the Abdominal and Pelvic Floor Muscles During Voluntary Exercises Neurourology and Urodynamics. 2001(20): 31-42. Sapsford RR, Hodges PW. Contraction of the pelvic floor muscles during abdominal maneuvers* 1. Archives of physical medicine and rehabilitation. 2001; 82(8): 1081-8. Neumann P, Gill V. Pelvic floor and abdominal muscle interaction: EMG activity and intra-abdominal pressure. International Urogynecology Journal. 2002; 13(2): 125-32. Arab AM, Behbahani RB, Lorestani L, Azari A. Assessment of pelvic floor muscle function in women with and without low back pain using transabdominal ultrasound. Manual therapy. 2010; 15(3): 235-9. Stokes M, Young A. Measurement of Quadriceps Cross– sectional Area by Ultrasonography: A Description of the Technique and its Applications in Physiotherapy. Informa Healthcare; 1986, pp. 31-6. Hodges P, Pengel L, Herbert R, Gandevia S. Measurement of muscle contraction with ultrasound imaging. Muscle and Nerve. 2003; 27(6): 682-92. McMeeken J, Beith I, Newham D, Milligan P, Critchley D. The relationship between EMG and change in thickness of transversus abdominis. Clinical Biomechanics. 2004; 19(4): 337-42. Costa LO, Maher CG, Latimer J, Hodges PW, D S. An investigation of the reproducibility of ultrasound measures of abdominal muscle activation in patients with chronic nonspecific low back pain. Eur Spine J. 2009; 18: 1059-65. Nourbakhsh MR, Arab AM. Relationship between mechanical factors and incidence of low back pain. The Journal of Orthopaedic and Sports Physical Therapy. 2002; 32(9): 447. Ainscough-Potts AM, Morrissey MC, Critchley D. The response of the transverse abdominis and internal oblique muscles to different postures. Manual Therapy. 2006; 11(1): 5460. Critchley D. Instructing pelvic floor contraction facilitates transversus abdominis thickness increase during low abdominal hollowing. Physiotherapy Research International. 2002; 7(2): 65-75. Ferreira PH, Ferreira ML, Hodges PW. Changes in recruitment of the abdominal muscles in people with low back pain: ultrasound measurement of muscle activity. Spine. 2004; 29(22): 2560. Teyhen DS, Gill NW, Whittaker JL, Henry SM, Hides JA, Hodges P. Rehabilitative ultrasound imaging of the abdominal muscles. The Journal of Orthopaedic and Sports Physical Therapy. 2007; 37(8): 450. Beith I, Synnott R, Newman S. Abdominal muscle activity during the abdominal hollowing manoeuvre in the four point kneeling and prone positions. Manual Therapy. 2001; 6(2): 82-7. Watkins MP, Library R. Foundations of clinical research: applications to practice: Pearson/Prentice Hall, 2009. Rankin G, Stokes M. Reliability of assessment tools in rehabilitation: an illustration of appropriate statistical analyses. Clinical Rehabilitation. 1998; 12(3): 187-99. Mannion AF, Pulkovski N, Gubler D, Gorelick M, O’Riordan D, Loupas T, et al. Muscle thickness changes during abdominal hollowing: An assessment of between-day measurement
N. Tahan et al. / Reliability of the ultrasound measurements of abdominal muscles activity
[33]
[34]
[35]
[36]
[37]
error in controls and patients with chronic low back pain. European Spine Journal. 2008; 17(4): 494-501. Critchley DJ, Coutts FJ. Abdominal Muscle Function in Chronic Low Back Pain Patients: Measurement with real-time ultrasound scanning. Physiotherapy. 2002; 88(6): 322-32. Teyhen DS, .Miltenberger CE, Delters HM, Deltoro YM, Pulliam JN, Childs J, et al. The use of ultrasound imaging of the abdominal drawing-in maneuver in subjects with low back pain. The Journal of Orthopaedic and Sports Physical Therapy. 2005; 35(6): 346-55. Bunce S, Moore A, Hough A. M-mode ultrasound: A reliable measure of transversus abdominis thickness? Clinical Biomechanics. 2002; 17(4): 315-7. Bunce S, Moore A, Hough A. M-mode ultrasound: A reliable measure of transversus abdominis thickness? Clin Biomech (Bristol, Avon). 2002; 17: 315-7. Hodges PW, Pengel LHM, Herbert RD, Gandevia SC. Measurement of muscle contraction with ultrasound imaging.
347
Wiley Online Library; 2003, pp. 682-92. Henry SM, Westervelt KC. The use of real-time ultrasound feedback in teaching abdominal hollowing exercises to healthy subjects. The Journal of Orthopaedic and Sports Physical Therapy. 2005; 35(6): 338-45. [39] Norasteh A, Ebrahimi E, Salavati M, Rafiei J, Abbasnejad E. Reliability of B-mode ultrasonography for abdominal muscles in asymptomatic and patients with acute low back pain. Journal of Bodywork and Movement Therapies. 2007; 11(1): 17-20. [40] Costa LOP, Maher CG, Latimer J, Smeets RJEM. Reproducibility of rehabilitative ultrasound imaging for the measurement of abdominal muscle activity: A systematic review. Physical therapy. 2009; 89(8): 756. [41] Cairns MC, Harrison K, Wright C. Pressure Biofeedback: A useful tool in the quantification of abdominal muscular dysfunction? Physiotherapy. 2000; 86(3): 127-38. [38]
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