LITERATURE REVIEW RELIABILITY OF SURFACE ELECTROMYOGRAPHY THE ASSESSMENT OF PARASPINAL MUSCLE FATIGUE: AN UPDATED SYSTEMATIC REVIEW
IN
Mohammad A. Mohseni Bandpei, PhD, a, b Nahid Rahmani, MSc, PT, c Basir Majdoleslam, PhD, d Iraj Abdollahi, PhD, e , ⁎ Shabnam Shah Ali, MSc, PT, f and Ashfaq Ahmad, DPT g
ABSTRACT Objective: The purpose of this study was to review the literature to determine whether surface electromyography (EMG) is a reliable tool to assess paraspinal muscle fatigue in healthy subjects and in patients with low back pain (LBP). Methods: A literature search for the period of 2000 to 2012 was performed, using PubMed, ProQuest, Science Direct, EMBASE, OVID, CINAHL, and MEDLINE databases. Electromyography, reliability, median frequency, paraspinal muscle, endurance, low back pain, and muscle fatigue were used as keywords. Results: The literature search yielded 178 studies using the above keywords. Twelve articles were selected according to the inclusion criteria of the study. In 7 of the 12 studies, the surface EMG was only applied in healthy subjects, and in 5 studies, the reliability of surface EMG was investigated in patients with LBP or a comparison with a control group. In all of these studies, median frequency was shown to be a reliable EMG parameter to assess paraspinal muscles fatigue. There was a wide variation among studies in terms of methodology, surface EMG parameters, electrode location, procedure, and homogeneity of the study population. Conclusions: The results suggest that there seems to be a convincing body of evidence to support the merit of surface EMG in the assessment of paraspinal muscle fatigue in healthy subject and in patients with LBP. (J Manipulative Physiol Ther 2014;37:510-521) Key Indexing Terms: Electromyography; Reliability; Low Back Pain; Muscle Fatigue; Review; Systematic
ow back pain (LBP) is a common and complicated disorder with reported high prevalence rates in many countries. 1 -4 Almost 80% of people will have at least 1 episode of LBP in their lifetime, 5 and 30% to 40% will experience LBP each year. 2,6 In Iran, LBP was reported to be one of the most common conditions affecting all populations with different prevalence rates, ranging from 17% for school children, 62% for nurses to more than 80% for pregnant
L a
Professor, Iranian Research Centre on Aging, Department of Physiotherapy, University of Social Welfare and Rehabilitation Sciences, Evin, Tehran, Iran. b Visiting Professor, University Institute of Physical Therapy, Faculty of Allied Health Sciences, University of Lahore, Lahore, Pakistan. c PhD Student, Department of Physiotherapy, University of Social Welfare and Rehabilitation Sciences, Tehran, Iran. d Assistant Professor, Department of Physiotherapy, University of Social Welfare and Rehabilitation Sciences, Tehran, Iran. e Assistant Professor, Department of Physiotherapy, University of Social Welfare and Rehabilitation Sciences, Tehran, Iran.
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women and surgeons. 3,7-9 Low back pain is one of the most common reasons for seeking medical care. 10 It is a costly condition with short- and long-term absenteeism and early retirement. 5,11 Low back pain was reported to be the main cause for 33.7% of work absenteeism during the past month in Iranian nurses. 3 Many causes such as anatomical, biomechanical, and psychophysiological factors were suggested for LBP. 12,13 In addition to degeneration of the lumbar spine, f
PhD Student, Department of Physiotherapy, University of Social Welfare and Rehabilitation Sciences, Tehran, Iran. g Assistant Professor, Department of Physical Therapy, University Institute of Physical Therapy, University of Lahore, Lahore, Pakistan. Submit requests for reprints to: Iraj Abdollahi, Assistant Professor, Department of Physiotherapy, University of Social Welfare and Rehabilitation Sciences, Student Blvd, Evin, Tehran, Iran. (e-mail:
[email protected]). Paper submitted December 16, 2013; in revised form April 28, 2014; accepted May 1, 2014. 0161-4754 Copyright © 2014 by National University of Health Sciences. http://dx.doi.org/10.1016/j.jmpt.2014.05.006
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reduced muscle strength and endurance and impaired function are also common in patients with chronic LBP. 14,15 There is adequate evidence to suggest that highly fatigable back muscles may predispose individuals to the development of LBP. 16,17 Although the exact pathophysiology of LBP is still not clearly understood, it seems that evaluation of paraspinal muscles is of great value in the assessment of such patients. Among available objective methods, magnetic resonance imaging, 18 ultrasonography, 19,20 and needle and surface electromyography (EMG) 21-24 have become increasingly common methods to assess muscle dimension and activity in healthy subjects and in patients with LBP. Despite many studies carried out in this area, the superior method is yet to be demonstrated in terms of being reliable, valid, convenient, noninvasive, and easily available to use. Surface EMG appears to be more convenient for both the patients and the researchers to analyze lower back muscles fatigue in laboratory studies and in clinical trials. 25 Despite suggested potential usefulness of the surface EMG approach in previous studies, this technique still reveals limitations in repeatability, reliability, and sensitivity to electrode location and type of muscle contraction and others. 25 Of various accessible techniques for using surface EMG, power spectral analysis, which focuses mainly on a single frequency parameter, the median frequency, as a measure of muscle function, is frequently used to evaluate muscle fatigue in healthy subjects and in patients with chronic LBP. 26-29 As the energy of muscle has a frequency spectrum, the surface EMG signal can be displayed with its range of frequencies. The power spectrum is the distribution of frequency components of the surface EMG signals. 26-29 As the muscle becomes fatigued, the median frequency of the EMG power spectrum shifts to lower frequencies due to altered muscle fiber recruitment and other changes in the contractile properties. 30,31 A number of shortcomings were found in the methodology of previous studies, which might help to understand some of the differences in conclusions of these studies. Some of them are as follows: 1. 2. 3. 4. 5.
Small sample size. Lack of a homogenous study population. Different definitions provided for LBP. Lack of valid and reliable or sensitive EMG parameters. Lack of a standard method for evaluating paraspinal muscle function and fatigue. 6. Lack of a standardized location for electrodes. The purpose of this study was to systematically review the previously published studies (2000-2012) concerning the reliability of surface EMG to assess lower back muscle fatigue in healthy subjects and in patients with chronic LBP. As published articles from 1985 to 1999 concerning the application of surface EMG in the assessment of LBP were included in the previous review of the first author and his colleagues, 24 the current review was performed on studies published from 2000 to 2012.
Mohseni Bandpei et al Surface EMG and Muscle Fatigue
METHODS The present systematic review was conducted according to the guideline of the Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA). 32 The study was given ethical approval from the University of Social Welfare and Rehabilitation Sciences.
Search Strategy To identify studies concerning the reliability of surface EMG in the assessment of lower back muscle fatigue, a literature search was carried out for the period of 2000 to 2012, using PubMed, Science Direct, OVID, EMBASE, MEDLINE, CINAHL, and ProQuest databases. The search strategy was used according to the PRISMA statements, using the following items: participants, interventions, comparisons, outcomes, and study design. The following keywords were also used: “para spinal muscles,” “electromyography,” “muscle fatigue,” “endurance,” “median frequency,” “low back pain,” and “reliability.” In addition, references given in the relevant publications were also searched.
Study Selection Inclusion Criteria. A literature search was performed to locate the relevant articles. The inclusion criteria of studies were as follows: 1. The reliability of surface EMG was investigated. 2. Paraspinal muscles were assessed. 3. Surface EMG was used to assess muscle fatigue in healthy subjects and/or in patients with chronic LBP. 4. Studies were published in English language.
Exclusion Criteria. Studies in which needle EMG was used, muscles other than paraspinal were assessed, and muscle fatigue was not investigated and which was not in English language were excluded. Data Extraction and Methodological Quality Two reviewers (NR and ShShA) independently selected potentially relevant studies from different databases. Disagreements were discussed until consensus was reached. Studies were included if they met all mentioned 4 inclusion criteria. If based on the title and abstract, it was not clear whether an article should be included, the whole article was checked (Fig). These 2 reviewers also read all the abstracts, and the third and fourth reviewers (MAMB and BM) separately have read a random sample of the abstracts. A consensus meeting was arranged to reach agreement on any differences among all reviewers. The outcome of a study was identified as “positive” if the authors concluded that surface EMG is a reliable method to assess paraspinal muscle fatigue in patients with LBP, in healthy subjects, or in a specific group or particular
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• • •
Fig. The PRISMA flowchart of study selection process. PRISMA, Preferred Reporting Items for Systematic Reviews and Meta-Analysis. condition of the study population. The outcome of a study was classified as “negative” if the authors concluded that surface EMG is not a reliable method to assess paraspinal muscle fatigue. These definitions of the “positive” and “negative” are used throughout this article.
RESULTS The literature search yielded 178 potentially eligible articles on the application of surface EMG in the assessment of lower back muscles. Of these, 153 were excluded based on title and abstract, leaving 25 studies to be read in full. The inclusion criteria were only met by 12 articles. 22,23,33-42 No additional articles were identified through the manual search. Table 1 shows details of the studies in chronological order from 2000 to 2012. The most important reasons for exclusion were that the article was not in English language; paraspinal muscles were not assessed, needle EMG was used, abstracts presented at different congresses without available full text, and muscle fatigue was not studied. In 7 of the 12 studies, the surface EMG was only applied in healthy subjects 22,23,33-36,39 (Table 2), and in 5 studies, the reliability of surface EMG was investigated in patients with LBP or a comparison with a control group 37,38,40-42 (Table 3).
In all of these studies, median frequency was shown to be a reliable EMG parameter to assess paraspinal muscles fatigue. Of the 12 studies that investigated the reliability of EMG, 3 studies compared the median frequency of surface EMG between healthy subjects and chronic LBP patients. Of the 12 studies, 4 studies considered only median frequency parameter for assessing the paraspinal muscle fatigue. 23,36,39,41 Four studies compared the 2 methods of EMG measures for evaluating muscle fatigue reliability including median frequency and root mean square (RMS). 22,35,37,38 The remaining 4 studies demonstrated a comparison between median frequency and mean power frequency, integrated rectified EMG (IREMG), and the entropy of the EMG methods. 32,33,40,42
DISCUSSION The present study was carried out to systematically review published studies from 2000 to 2012 concerning the reliability of surface EMG to assess lower back muscle fatigue in healthy subjects and in patients with chronic LBP. Twelve studies were met the inclusion criteria and were reviewed. Despite some methodological flaws identified in previous studies such as small sample size, heterogeneous sample, lack of
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Table 1. Details of Studies Investigating the Reliability of Surface EMG in Lower Back Muscles Authors
Purpose
Subject
Test/Posture
Electrode Location
Dedering et al33
To evaluate the test-retest reliability of common methods of examining muscle fatigue
10 Healthy (2 males, 8 females)
Modified Sorensen test on 3 separate days within 3-wk period
Erector spinae muscle/ L1, L5 level
Koumantakis et al22
To compare the 16 Healthy accuracy and (7 males, test-retest reliability 9 females) of SEMG for back muscle endurance assessment
Modified Sorensen test in upright position on 4 separate days within 3-wk period
Bilateral erector spinae (L2/L3), multifidus (L4/L5)
Koumantakis et al34
To evaluate the 20 Healthy test-retest reliability (10 males, of SEMG to assess 10 females) endurance of the multifidus muscle
10-s high-intensity Unilateral multifidus voluntary (L4/L5) contractions from 4-point kneeling position on 3 d within 1-wk period
Mohseni-Bandpei To determine and Watson23 the test-retest reliability of SEMG of paraspinal muscle fatigue
15 Healthy (6 males, 9 females)
Modified Sorensen Multifidus test on 3 sessions (L1/L2), within 1-wk period iliocostalis lumbarom (L2)
Arnall et al35
To investigate the 10 Healthy test-retest reliability (6 males, of paraspinal 4 females) muscle fatigue
60-s isometric contractions at 40%, 50%, and 60% MVC force on 2 sessions within 3 d
Paraspinal muscles/L4-L5, L2-L3
Ebenbichler et al36
To assess the 14 Healthy test-retest reliability males of time-frequency EMG measures during dynamic and static lifting
Dynamic and static lifting tests on 3 sessions within 2-wk period
Paraspinal muscles at T10, L2, L5 levels and UT, BF, VL
EMG Parameters
Conclusion
MF, MFS, The method MF at different used for assessing Borg ratings para spinal muscle fatigue proved to be reliable. (ICC, 0.65-0.90 for the slope of the total time; ICC, 0.75-0.89 for the initial and end MF; ICC, 0.63-0.88 for MF at different Borg ratings) MF, MFS, MF and MFS and RMS were more reliable than RMS (ICC, 0.79-0.97 for MF; ICC, 0.52-0.84 for MFS; ICC, 0.51-0.74 for RMS) MF, IREMG The reliability was moderate for MF and was poor for IREMG (ICC, 0.48-0.67 for MF; ICC, − 0.0025 to 0.18 for IREMG) MF, MFS SEMG was shown to be a reliable method of evaluating back extensor muscle activity and fatigue (ICC, 0.71-0.88 for MF; ICC,0.60-0.85 for MFS) MF, MFS, The most reliability and RMS for MF was shown at 50% MVC force. MF and RMS were found not suitable for assessing muscle fatigue (ICC, 0.74-0.86 for MF; ICC,0.60-0.85 for RMS; ICC, 0.26-0.77 for MFS) IMDF and The time-frequency time-dependent EMG measurements changes were shown to be a reliable method (ICC, 0.89.5-0.99 reported at different electrode sites for IMDF; ICC, 0.45.4-0.100 reported (continued on next page)
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Table 1. (continued) Authors
Purpose
Subject
Test/Posture
Electrode Location
EMG Parameters
Lariviere et al37
To assess the test-retest reliability of different EMG indices for the evaluation of impaired back muscles
20 Healthy (male and female) and 20 CLBP (male)
Two static trunk Multifidus (L5), extension tasks iliocostalis (L3), at 75% of the longissimus MVC in a static (L1, T10) dynamometer on 3 sessions within 2-wk period
MF, RMS
Lariviere et al38
To investigate the test-retest reliability of EMG for the assessment of back and abdominal muscles
20 Healthy (male and female) and 20 CLBP (male)
Maximal and submaximal static trunk extension tasks in a static dynamometer on 3 sessions within 2-wk period
Multifidus (L5), iliocostalis (L3), longissimus (T10), abdominal muscles at L4 (RA, EO, IO)
RMS, MF
Coorevits et al39
To evaluate the test-retest reliability of EMG measurements of back and hip muscles
20 Healthy (10 males, 10 females)
Isometric back extensions (modified Sorensen test) on 2 separate days within 1-wk period
MF, IMDF Latissimus dorsi, longissimus thorasis, iliocostalis lumbarom, multifidus, gluteus maximus, BF
Lariviere et al40
To assess test-retest reliability of EMG variables of muscle fatigue
20 Healthy (male and female) and 20 CLBP (male)
Multifidus (L5), iliocostalis lumbarom (L3), longissimus (L1, T10)
RMS
Dedering et al41
To assess the test-retest reliability of MF, endurance time, and ratings of lumbar muscle fatigue
15 patients with lumbar disc herniation
Three MVC and endurance test while standing in a static dynamometer on 3 sessions within 2-wk period Modified Sorensen test on 3 times within 2-wk period
Lumbar erector spinae muscles
MF
Conclusion at different electrode sites for time trends) Medial back muscles showed more reliability in both groups and the reliability of EMG can be increased by averaging data (mean ICC, 0.76 and 0.82 for initial MF in healthy subjects and CLBP, respectively; mean ICC, 0.47 and 0.46 for RMS in healthy subjects and CLBP, respectively) Only the EMG indices based on MF estimates showed acceptable reliability. The most reliable EMG indices were the bilateral average of medial back muscles (ICC, 0.68-0.91) and the average of all back muscles (ICC, 0.77-0.91). Both EMG parameters were shown to be reliable in the analysis of back and hip muscle fatigue during an isometric back extension test (ICC, 0.443-0.727 for IMDF slope; ICC, 0.273-0.734 for MF slope) The reliability of EMG ratio variables ranged from moderate to excellent (ICC, 0.50-0.91)
Endurance time and MF showed good and acceptable reliability, respectively (ICC, 0.85 for endurance time; ICC N0.06 for MF)
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Table 1. (continued) Authors
Purpose
Subject
Test/Posture
Electrode Location
Sung et al42
To evaluate between days reliability of SEMG variables in muscle fatigability
32 LBP (16 males, 16 females)
Submaximal Erector spinae contraction (L4/L5) in modified Sorensen test on 2 sessions within 1-wk period
EMG Parameters MF, MFS, and entropy of the EMG
Conclusion The entropy analysis could be a more reliable measure of muscle fatigue compared with MF and MFS (ICC, 0.82-0.85 for entropy analysis; ICC, 0.54-0.64 for MF; ICC, 0.26-0.30 for MFS)
BF, biceps femoris; CLBP, chronic low back pain; EMG, electromyography; EO, external oblique; ICC, intraclass correlation coefficient; IMDF, instantaneous median frequency; IO, internal oblique; IREMG, integrated rectified electromyography; LBP, low back pain; MF, median frequency; MFS, median frequency slope; MVC, maximum voluntary isometric contraction; RA, rectus abdominis; RMS, root mean square; SEMG, surface electromyography; UT, upper trapezius; VL, vastus lateralis.
standardized location for electrode, and others, the results of this review indicate that surface EMG can be considered as a useful and reliable tool to evaluate paraspinal muscle fatigue in healthy subjects and in patients with LBP. Although the etiology of LBP is still controversial, it was suggested that subjects with LBP have less endurance during sustained muscle contraction, 26,28 and poor back extensor muscle is a predictor for the occurrence of LBP. 17,43 A large amount of studies were conducted to find the link between LBP and fatigue using surface EMG. 24 According to the results of this study, different EMG parameters including median frequency, instantaneous median frequency, median frequency slope, root mean square, and IREMG were used to measure the paraspinal muscle fatigue. There were also different protocols reported such as Biering-Sorensen test, isometric contraction in different positions, static trunk extension at different levels of maximum voluntary contraction, and maximal and submaximal trunk extension task. Despite the variability of EMG parameters among studies with different reported conclusions ( Table 1), median frequency parameter was found to be a relatively more reliable EMG parameter compared with other variables in the evaluation of paraspinal muscle fatigue. Among different muscle fatigue evaluation protocols, BieringSorensen test was found to be more appropriate in the assessment of paraspinal muscle fatigue. 44,45
Reliability of Surface EMG on Muscle Fatigue in Healthy Subjects Many studies were found using surface EMG in the assessment of paraspinal muscles fatigue in healthy subjects applying different EMG parameters. In this systematic review, 7 studies applied EMG in the assessment of muscle fatigue in healthy subjects. Dedering et al 33 investigated the reliability of median frequency and mean power frequency of surface EMG to examine lower back erector spinae muscles fatigue during the modified test. Higher reliability score was reported for total median frequency slope
compared with the median frequencies at the beginning and at the end. Good reliability was shown for endurance time, the initial and end median and mean power frequencies, and median and mean power frequencies. In the study carried out by Koumantakis et al, 22 the reliability of surface EMG in the assessment of erector spinae muscles endurance and fatigue was investigated during 60second isometric contraction of using isomyometer device. Median frequency slope appeared to be more reliable than RMS at the 60% maximum voluntary isometric contraction (MVC) in their study. Koumantakis et al 34 also investigated the reliability of surface EMG to evaluate the multifidus muscle endurance during intermittent isometric exercise. Good reliability was reported for median frequency and IREMG. For both EMG parameters, the reliability of endurance test was moderate. Mohseni-Bandpei and Watson 23 have studied the testretest reliability of surface EMG in the assessment of paraspinal fatigue during Sorensen test. The median frequency slope was shown to be a more reliable method to monitor paravertebral muscles (multifidus and iliocostalis) fatigue. Within-day reliability measurements of median frequency slope were moderate to high for both muscles, whereas between-days reliability of median frequency slope was shown to be high for multifidus and moderate for iliocostalis. The reliability of surface EMG on paraspinal muscles at 40%, 50%, and 60% MVC force during 60-second isometric contractions was also investigated by Arnall et al. 35 The initial median frequency, median frequency slope, and RMS measures were analyzed. Excellent reliability was reported at 50% MVC force, and initial median frequency and RMS were shown to be more reliable than median frequency slope. Ebenbichler et al 36 studied the reliability of time frequency EMG in the assessment of paraspinal muscles fatigue during repetitive dynamic lifting in comparison with the reliability of median frequency measures of fatigue during static lifting. High reliability was
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Table 2. Details of Studies Investigated the Reliability of Surface EMG in Healthy Subjects Purpose
Dedering et al33
To evaluate the 10 Healthy test-retest reliability (2 males, of common methods 8 females) of examining muscle fatigue
Modified Sorensen Erector spinae test on 3 separate muscle/L1, days within L5 level 3-wk period
MF, MFS, MF at different Borg ratings
Koumantakis et al22
To compare the accuracy and test-retest reliability of SEMG for back muscle endurance assessment
16 Healthy (7 males, 9 females)
Modified Bilateral erector Sorensen spinae (L2/L3), test in upright multifidus (L4/L5) position on 4 separate days within 3-wk period
MF, MFS, and RMS
Koumantakis et al34
To evaluate the test-retest reliability of SEMG to assess endurance of the multifidus muscle
20 Healthy 10-s high-intensity (10 males, voluntary 10 females) contractions from 4-point kneeling position on 3 d within 1-wk period 15 Healthy Modified (6 males, Sorensen test 9 females) on 3 sessions within 1-wk period
Mohseni-Bandpei To determine the and Watson23 test-retest reliability of SEMG of paraspinal muscle fatigue
Subject
Test/Posture
Electrode Location
EMG Parameters
Authors
Unilateral multifidus (L4/L5)
MF, IREMG
Multifidus (L1/L2), iliocostalis lumbarom (L2)
MF, MFS
Arnall et al35
To investigate the test-retest reliability of paraspinal muscle fatigue
10 Healthy (6 males, 4 females)
60-s isometric Para spinal contractions 4t muscles/L4-L5, 40%, 50%, L2-L3 60% MVC force on 2 sessions within 3 d
Ebenbichler et al36
To assess the test-retest reliability of time-frequency EMG measures during dynamic and static lifting
14 Healthy males
Dynamic and static lifting tests on 3 sessions within 2-wk period
Paraspinal muscles at T10, L2, L5 levels and UT, BF, VL
Coorevits
To evaluate the
20 Healthy
Isometric back
Latissimus dorsi,
Conclusion The method used for assessing paraspinal muscle fatigue proved to be reliable (ICC, 0.65-0.90 for the slope of the total time; ICC, 0.75-0.89 for the initial and end MF; ICC, 0.63-0.88 for MF at different Borg ratings) MF and MFS were more reliable than RMS (ICC, 0.79-0.97 for MF; ICC, 0.52-0.84 for MFS; ICC, 0.51-0.74 for RMS) The reliability was moderate for MF and was poor for IREMG (ICC, 0.48-0.67 for MF; ICC, − 0.0025 to 0.18 for IREMG)
SEMG was shown to be a reliable method of evaluating back extensor muscle activity and fatigue. (ICC, 0.71-0.88 for MF; ICC, 0.60-0.85 for MFS) MF, MFS, and RMS The most reliability for MF was shown at 50% MVC force. MF and RMS were found not suitable for assessing muscle fatigue (ICC, 0.74-0.86 for MF; ICC, 0.60-0.85 for RMS; ICC, 0.26-0.77 for MFS) IMDF and The time-frequency time-dependent EMG measurements changes were shown to be a reliable method (ICC, 0.89.5-0.99 reported at different electrode sites for IMDF; ICC, 0.45.4-0.100 reported at different electrode sites for time trends) MF, IMDF Both EMG parameters
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Table 2. (continued) Authors et al39
Purpose
Subject
Test/Posture
test-retest reliability of EMG measurements of back and hip muscles
(10 males, extensions 10 females) (modified Sorensen test) on 2 separate days within 1-wk period
Electrode Location longissimus thorasis, iliocostalis lumbarom, multifidus, gluteus maximus, BF
EMG Parameters
Conclusion were shown to be reliable in the analysis of back and hip muscle fatigue during an isometric back extension test. (ICC, 0.443-0.727 for IMDF slope; ICC, 0.273-0.734 for MF slope)
BF, biceps femoris; EMG, electromyography; ICC, intraclass correlation coefficient; IMDF, instantaneous median frequency; IREMG, integrated rectified electromyography; MF, median frequency; MFS, median frequency slope; MVC, maximum voluntary isometric contraction; RMS, root mean square; SEMG, surface electromyography; UT, upper trapezius; VL, vastus lateralis.
demonstrated for instantaneous median frequency (IMF) and its time-dependent changes during dynamic lifting and in the comparison with median frequency; both methods had equally good reliability. Coorevits et al 39 investigated the test-retest reliability of median frequency and IMF in the assessment of back and hip muscles fatigue during Sorensen test. They determined that both methods of fatigue evaluation had generally good reliability. The more medially located back muscles showed more reliability than those located more laterally. Hip muscles demonstrated lower reliability compared with back muscles.
Reliability of Surface EMG on Muscle Fatigue in Patients With Chronic LBP Previous studies reported that maximal performance measurement (strength and endurance) depends heavily on many factors including the capacity of subjects to activate all motor units. 44 -46 This has been considered as a difficult task for patients with chronic LBP and might explain the variability in the EMG signal caused by variability of load sharing 47,48 and also poor reliability results reported on EMG fatigue parameters. 49,50 This is why the reliability of surface EMG on muscle fatigue in patients with chronic LBP is discussed separately. Three studies were carried out by Lariviere et al 37,38,40 to determine the reliability of surface EMG in the assessment of paraspinal muscles fatigue in patients with chronic LBP compared with healthy subjects. In 2002, they studied the reliability of 2 methods of fatigue evaluation including median frequency and RMS during 2 static trunk extension tasks at 75% MVC and their time-dependent changes with 5-second recovery time. For both groups, the control subjects and chronic LBP patients, similar reliability was shown for median frequency slope. Median frequency slope index was superior relative to RMS, which demonstrated
poor reliability. Median frequency slope for muscles located medially was more reliable than those located more laterally, and these data were consistent to the study conducted by Coorevits et al. 39 They have reported that the reliability of surface EMG parameters may increase by averaging across bilateral muscles, electrode positioned at different vertebral levels, and the measurements of 2 endurance tests performed within 1 session. In another study, Larriviere et al 38 investigated the reliability and sensitivity of surface EMG in the assessment of back muscle fatigue, weakness, and fiber composition between healthy subjects and patients with chronic LBP during a maximal and submaximal static trunk extension tasks. Median frequency and RMS were analyzed. Similar reliability was showed in both healthy and chronic LBP groups for all EMG parameters. In the assessment of muscle weakness, in both healthy and chronic LBP groups, averaging values of EMG showed good to excellent reliability. In the evaluation of muscle fiber composition and muscle fatigue, excellent and acceptable reliabilities were reported for both groups, respectively. Measurements of medial muscles seemed to be more reliable compared with those muscles located laterally. Larriviere et al 40 investigated the reliability of surface EMG in the evaluation of paraspinal muscles endurance during static trunk extension test. Root mean square and amplitude values were computed and analyzed at each force level from 10% to 80% and for each step contraction (10%, 20%, 40%, 60%, and 80% MVC). This study showed more reliability for medially located muscles than those located laterally, and more activity was observed at low to moderate force levels compared with high force levels, which demonstrated more variability. The good to excellent reliability was reported in approximately 60% of the test conditions, and for the other test conditions, moderated reliability was shown.
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Table 3. Details of Studies Investigated Muscle Fatigue in Patients With LBP Compared With Healthy Subjects EMG Parameters
Authors
Purpose
Subject
Test/Posture
Electrode Location
Lariviere et al37
To assess the test-retest reliability of different EMG indices for the evaluation of impaired back muscles
20 Healthy (male and female) and 20 CLBP (male)
Two static trunk extension tasks at 75% of the MVC in a static dynamometer on 3 sessions within 2-wk period
Multifidus (L5), iliocostalis (L3), longissimus (L1, T10)
MF, RMS
Lariviere et al38
To investigate the test-retest reliability of EMG for the assessment of back and abdominal muscles
20 Healthy (male and female) and 20 CLBP (male)
Maximal and submaximal static trunk extension tasks in a static dynamometer on 3 sessions within 2-wk period
Multifidus (L5), iliocostalis (L3), longissimus (T10), abdominal muscles at L4 (RA, EO, IO)
RMS, MF
20 Healthy (male and female) and 20 CLBP (male)
Three MVC and endurance test while standing in a static dynamometer on 3 sessions within 2-wk period Modified Sorensen test on 3 times within 2-wk period
Multifidus (L5), RMS iliocostalis lumbarom (L3), longissimus (L1, T10)
Lariviere To assess et al40 test-retest reliability of EMG variables of muscle fatigue
Dedering To assess the 15 patients with et al41 test-retest reliability lumbar disk of MF, endurance herniation time, and ratings of lumbar muscle fatigue
Sung et To evaluate al42 between days reliability of SEMG variables in muscle fatigability
Lumbar erector spinae muscles
32 LBP (16 males, Submaximal Erector spinae 16 females) contraction (L4/L5) in modified Sorensen test on 2 sessions within 1-wk period
Conclusion Medial back muscles showed more reliability in both groups and the reliability of EMG can be increased by averaging data (mean ICC, 0.76 and 0.82 for initial MF in healthy subjects and CLBP, respectively; mean ICC, 0.47 and 0.46 for RMS in healthy subjects and CLBP, respectively) Only the EMG indices based on MF estimates showed acceptable reliability. The most reliable EMG indices were the bilateral average of medial back muscles (ICC, 0.68-0.91) and the average of all back muscles (ICC, 0.77-0.91). The reliability of EMG ratio variables ranged from moderate to excellent (ICC, 0.50-0.91)
MF
Endurance time and MF showed good and acceptable reliability, respectively. (ICC, 0.85 for endurance time; ICC N0.06 for MF) MF, MFS, The entropy analysis could and entropy of be a more reliable the EMG measure of muscle fatigue compared with MF and MFS (ICC, 0.82-0.85 for entropy analysis; ICC, 0.54-0.64 for MF; ICC, 0.26-0.30 for MFS)
CLBP, chronic low back pain; EMG, electromyography; EO,external oblique; ICC, intraclass correlation coefficient; IO, internal oblique; LBP, low back pain; MF, median frequency; MFS, median frequency slope; MVC, maximum voluntary isometric contraction; RA, rectus abdominis; RMS, root mean square; SEMG, surface electromyography.
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Dedering et al 41 investigated the reliability of power spectral analysis of EMG measures and endurance test in the evaluation of back muscles fatigue in patients with lumbar disk herniation during a modified Sorensen test. Good, acceptable, and poor reliabilities were reported for endurance time, median frequency, and median frequency slope, respectively. It was suggested to use endurance time to monitor the effect of different interventions in patients with LBP. The reliability of surface EMG in the assessment of erector spinae muscles fatigue in patients with LBP during Sorensen test was also studied by Sung et al. 42 Median frequency, median frequency slope, and entropy of the EMG time series information were analyzed. Generally, the entropy measures of EMG for erector spinae muscles were more reliable than median frequency and median frequency slope. However, although the methodology to conduct this systematic review was improved compared with our previous review, the conclusions of this update do not differ, and the general picture of the reliability of surface EMG has not changed since then. Based on the methodologic quality assessment, the new studies in this review had no higher methodologic quality than the studies of the earlier review. The most prevalent shortcomings such as small sample size, heterogeneous sample, lack of standardized location for electrode, differences in degree and source of pain, combinations of various subgroups of LBP patients, and others, which could easily have been avoided, still exist.
Mohseni Bandpei et al Surface EMG and Muscle Fatigue
which reflect paraspinal muscle fatigue during different tasks and positions. Within-day reliability showed more satisfactory results compared with between-days reliability measurements. Many factors including the lack of standardized EMG protocols, the type, size and location of electrodes, interelectrode distances, the temperature of the muscle and skin, the force produced by the muscle contraction particularly in patients with pain, muscle fiber composition and blood flow, fat layer thickness, and others may all affect the quality of signals and measurements using surface EMG and making comparisons across people, tasks, days, and muscle groups difficult.
Practical Applications • Surface EMG may be as a useful tool to diagnose muscle fatigue and to monitor the effect of different interventions. • The most commonly used surface EMG parameters were median frequency, mean power frequency, RMS, and IMF, which reflect paraspinal muscle fatigue during different tasks and positions.
LIMITATIONS A few limitations need to be considered when interpreting the results of present review. For this review, only studies evaluating the reliability of surface EMG on healthy subjects and patients with LBP were included, and consequently, generalization to other healthy or clinical populations may be limited. Only reliability of surface EMG recorded for spinal muscles was assessed, and other studies evaluating the possible contribution and fatigue of other muscles including lower limb muscles were not included. It is possible that the result is overestimated in this review because of publication bias. The language criteria used for including studies in this review might even have enlarged this risk, as positive results are more likely to be published in English. However, it was not possible to estimate the impact that it might have had on the results. Meanwhile, the current review aimed at the reliability of surface EMG in the assessment of paraspinal muscle fatigue; however, the validity of surface EMG remains an area to be more investigated in evaluating paraspinal muscle fatigue.
However, despite all variations and shortcomings in reviewed studies, it seems that surface EMG may be considered as a useful tool to diagnose muscle fatigue and to monitor the effect of different interventions used to improve the muscle endurance and reduce the muscle fatigue. As far as the EMG parameters are concerned, median frequency was found to be relatively more reliable compared with other variables to evaluate lower back muscles fatigue in healthy subjects or patients with LBP. Further studies are still needed to find the most reliable approach and EMG parameter in the assessment of paraspinal muscle fatigue.
CONCLUSION
CONTRIBUTORSHIP INFORMATION
The most commonly used surface EMG parameters were median frequency, mean power frequency, RMS, and IMF,
FUNDING SOURCES AND POTENTIAL CONFLICTS OF INTEREST The current study was financially supported by the University of Social Welfare and Rehabilitation Sciences (Student Research Committee). No conflicts of interest were reported for this study.
Concept development (provided idea for the research): M.A.M.B., N.R., B.M., I.A.
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Mohseni Bandpei et al Surface EMG and Muscle Fatigue
Design (planned the methods to generate the results): M. AM.B., N.R., BM., I.A., S.S.A. Supervision (provided oversight, responsible for organization and implementation, writing of the manuscript): M.A.M.B., B.M., I.A. Data collection/processing (responsible for experiments, patient management, organization, or reporting data): MA.M.B., N.R., B.M.I.A., S.S.A., M.B. Analysis/interpretation (responsible for statistical analysis, evaluation, and presentation of the results): M.A.M. B., N.R., B.M., I.A., S.S.A. Literature search (performed the literature search): M.A. M.B., N.R., B.M., I.A., S.S.A., A.A., M.B. Writing (responsible for writing a substantive part of the manuscript): M.A.M.B., N.R., B.M., I.A., S.S.A., A.A. Critical review (revised manuscript for intellectual content, this does not relate to spelling and grammar checking): M.A.M.B., N.R., B.M., I.A., A.A.
REFERENCES 1. Maniakis A, Gray A. The economic burden of back pain in the UK. Pain 2000;84:95-103. 2. Worku Z. Prevalence of low back pain in Lesotho mothers. J Manipulative Physiol Ther 2000;23:147-54. 3. Mohseni-Bandpei MA, Fakhri M, Shirvani M, et al. Occupational low back pain in Iranian nurses: an epidemiological study. Br J Nurs 2006;15:914-7. 4. Walker BF. The prevalence of LBP. A systematic review of the literature from 1966 to 1998. J Spinal Disord 2000;13:205-17. 5. Airaksinen O, Brox JI, Cedraschi C, et al. Chapter 4. European guidelines for the management of chronic nonspecific low back pain. Eur Spine J 2006;15(Suppl 2):S192-300. 6. Waddell G, Burton AK. Occupational health guidelines for the management of low back pain. Occup Med 2001;51:124-35. 7. Mohseni-Bandpei MA, Bagheri Nessami M, Shayesteh Azar M. Nonspecific low back pain in 5000 Iranian school age children. J Pediatr Orthop 2007;27:126-9. 8. Mohseni-Bandpei M, Fakhri M, Ahmad-Shirvani M, et al. Low back pain in 1100 Iranian pregnant women: prevalence and risk factors. Spine J 2009;9:795-801. 9. Mohseni-Bandpei MA, Ahmad-Shirvani M, Golbabaei N, Behtash H, Shahinfar Z, Fernandez-de-las-Penas C. Prevalence and risk factors associated with low back pain in Iranian surgeons. J Manipulative Physiol Ther 2011;34:362-70. 10. Licciardone JC. The epidemiology and medical management of low back pain during ambulatory medical care visits in the United States. Osteopath Med Prim Care 2008;2(11):1-17. 11. Wenig CM, Schmidt CO, Kohlmann Th, Schweikert B. Costs of back pain in Germany. Eur J Pain 2009;13:280-6. 12. Mannion AF. Fiber type characteristics and function of the human paraspinal muscles: normal values and changes in association with low back pain. J Electromyogr Kinesiol 1999;9:363-77. 13. Ng JKF, Richardson CA, Kippers V, Parnianpour M. Relationship between muscle fiber composition and functional capacity of back muscles in healthy subjects and patients with back pain. J Orthop Sports Phys Ther 1998;27:389-402. 14. Bartleson JD. Low back pain. Curr Treat Options Neurol 2001;3:159-68.
Journal of Manipulative and Physiological Therapeutics September 2014
15. Pope MH, Goh KL, Magnusson ML. Spine ergonomics. Annu Rev Biomed Eng 2002;4:49-68. 16. Biering-Sorensen F. Physical measurements as risk factors for low-back trouble over a year period. Spine 1984;9:106-19. 17. Adams MA, Mannion AF, Dolan P. Personal risk factors for first time low back pain. Spine 1999;24:2497-505. 18. Lewis SE, Fowler NE. Changes in intervertebral disk dimensions after a loading task and the relationship with stature change measurements. Arch Phys Med Rehabil 2009; 90:1795-9. 19. Ghamkhar L, Emami M, Mohseni-Bandpei MA, Behtash H. Application of rehabilitative ultrasound in the assessment of low back pain: a literature review. J Bodyw Mov Ther 2011; 15:465-77. 20. Javanshir K, Amiri M, Mohseni-Bandpei MA, Rezasoltani A, Fernández-de-las-Peñas C. Ultrasonography of the cervical muscles: a critical review of the literature. J Manipulative Physiol Ther 2010;33:630-7. 21. Lariviere C, Arsenault AB. On the use of EMG-ratios to assess the coordination of back muscles. Clin Biomech 2008;23: 1209-19. 22. Koumantakis GA, Arnall F, Cooper RG, Oldham JA. Paraspinal muscle fatigue testing with two methods in healthy volunteers. Reliability in the context of clinical applications. Clin Biomech 2001;16:263-6. 23. Mohseni-Bandpei MA, Watson M. Electromyographic power spectral analysis of the paraspinal muscles: a reliability study. Physiotherapy 2001;87:470-8. 24. Mohseni-Bandpei MA, Watson M, Richardson B. Application of surface electromyography in the assessment of low back pain: a literature review; Reliability study. Phys Ther 2000;5:93-105. 25. Farina D, Gazzoni M, Merletti R. Assessment of low back muscle fatigue by surface EMG signal analysis: methodological aspects. J Electromyogr Kinesiol 2003;13:319-32. 26. Sung P. The efficacy of median frequency on multifidi muscles during one-minute back extension. Arch Phys Med Rehabil 2003;84:1313-8. 27. Merletti R, Roy SH, Kupa E, Roatta S, Granata A. Modeling of surface myoelectric signals—part II: model-based signal interpretation. IEEE Trans Biomed Eng 1999;46:821-9. 28. Mannion AF, Connolly B, Wood K, Dolan P. The use of surface EMG power spectral analysis in the evaluation of back muscle function. J Rehabil Res Dev 1997;34:427-39. 29. Roy SH, De Luca CJ, Emley M, et al. Classification of back muscle impairment based on the surface electromyographic signal. J Rehabil Res Dev 1997;34:405-14. 30. Basmajian JV, De Luca CJ. Muscles alive. Baltimore: Williams& Wilkins; 1985. 31. De Luca CJ. Use of surface EMG signal for performance evaluation of back muscles. Muscle Nerve 1993;16:210-6. 32. Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. J Clin Epidemiol 2009;62:1006-12. 33. Dedering A, Hjelmsater M R, Elfving B, Ringdahl K H, Nemeth G. Between-days reliability of subjective and objective assessments of back extensor muscle fatigue in subjects without lower-back pain. J Electromyogr Kinesiol 2000;10:151-8. 34. Koumantakis GA, Oldham JA, Winstanley J. Intermittent isometric fatigue study of the lumbar multifidus muscle in four-point kneeling: an intra-rater reliability investigation. Man Ther 2001;6:97-105. 35. Arnall FA, Koumantakis GA, Oldham JA, Cooper RG. Between-days reliability of electromyographic measures of paraspinal muscle fatigue at 40, 50 and 60% levels of maximal voluntary contractile force. Clin Rehabil 2002;16:761-71.
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36. Ebenbichler GR, Bonato P, Roy SH, et al. Reliability of EMG time-frequency measures of fatigue during repetitive lifting. Med Sci Sports Exerc 2002;34:1316-23. 37. Lariviere C, Arsenault AB, Gravel D, Gagnon D, Loisel P. Evaluation of measurement strategies to increase the reliability of EMG indices to assess back muscle fatigue and recovery. J Electromyogr Kinesiol 2002;12:91-102. 38. Lariviere C, Arsenault AB, Gravel D, Gagnon D, Loisel P. Surface electromyography assessment of back muscle intrinsic properties. J Electromyogr Kinesiol 2003;13:305-18. 39. Coorevits P, Danneels L, Cambier D, et al. Test-retest reliability of wavelet and Fourier based EMG (instantaneous) median frequencies in the evaluation of back and hip muscle fatigue during isometric back extensions. J Electromyogr Kinesiol 2008;18:768-806. 40. Lariviere C, Gravel D, Gagnon D, Arsenault B. The assessment of back muscle capacity using intermittent static contractions. Part II: validity and reliability of biomechanical correlates of muscle fatigue. J Electromyogr Kinesiol 2008; 18:1020-31. 41. Dedering A, Gnospelius A, Elfving B. Reliability of measurements of endurance time, electromyographic fatigue and recovery, and associations to activity limitations, in patients with lumbar disc herniation. Physiother Res Int 2010;15:189-98. 42. Sung PS, Zurcher U, Kaufman M. Reliability difference between spectral and entropic measures of erector spinae muscle fatigability. J Electromyogr Kinesiol 2010;20:25-30.
Mohseni Bandpei et al Surface EMG and Muscle Fatigue
43. Luoto S, Heliovaara M, Hurri H, Alaranta H. Static back endurance and the risk of low back pain. Clin Biomech 1995;10:323-4. 44. Moureau CE, Green BN, Johnson CD, Moreau SR. Isometric back extension endurance tests: a review of the literature. J Manipulative Physiol Ther 2001;24:110-22. 45. Clark BC, Manini TM, Thé DJ, Doldo NA, Ploutz-Snyder LL. Gender differences in skeletal muscle fatigability are related to contraction type and EMG spectral compression. J Appl Physiol 2003;94:2263-72. 46. Demoulin C, Vanderthommen M, Duysens C, Crielaard JM. Spinal muscle evaluation using the Sorensen test: a critical appraisal of the literature. Joint Bone Spine 2006;73:43-50. 47. Mannion AF, Dumas GA, Stevenson JM, Cooper RG. The influence of muscle fiber size and type distribution on electromyographic measures of back muscle fatigability. Spine 1998;23:576-84. 48. Latimer J, Maher CG, Refshauge K, Colaco I. The reliability and validity of the Biering-Sorensen test in asymptomatic subjects and subjects reporting current or previous nonspecific low back pain. Spine 1999;24:2085-90. 49. Plamondon A, Trimble K, Larivière C, Desjardins P. Back muscle fatigue during intermittent prone back extension exercise. Scand J Med Sci Sports 2004;14:1-10. 50. Mayer JM, Verna JL, Manini TM, Mooney V, Graves JE. Electromyographic activity of the trunk extensor muscles: effect of varying hip position and lumbar posture during Roman chair exercise. Arch Phys Med Rehabil 2002;83:1543-6.
521