Surface EMG
Surface EMG
ABSTRACT
        Background: The validity and applicability of erector spinae electromyogram (EMG) use in clinical
        practice is questionable. Differences in the amplitude of the EMG signal between populations with low
        back pain (LBP) and controls have been hypothesized but not sufficiently documented.
        Objective: To examine issues of EMG asymmetry and repeatability in populations with LBP and
        populations without LBP in 3 separate studies.
        Study Design: Three separate experimental research studies.
        Methods: Study 1 examined the intraclass correlation of the EMG signal of the paraspinal musculature
        at L3 on 3 separate days during quiet stance with use of 3 different normalization techniques: percent
        maximum voluntary contraction, percent submaximal voluntary contraction, and percent averaged
        submaximal contractions. Study 2 used a population with chronic LBP to compare the bilateral
        asymmetry of paraspinal musculature in segments exhibiting pain with segments not exhibiting pain
        during quiet stance. A 1-way analysis of variance was used to compare differences between asymmetry
        scores in the pain and nonpain groups. In study 3, persons with LBP and persons in the control group had
        the dynamic asymmetry of paraspinal musculature compared during forward bending. A cross-correlation
        coefficient assessing bilateral muscle activity was calculated for each subject and differences between
        groups were evaluated using a 1-way analysis of variance.
        Results: Study 1: Subjects showed excellent repeatability (ICC ⬎ 0.75) regardless of the normalization
        technique. Study 2: During quiet stance no differences were found in bilateral asymmetry between painful
        and nonpainful motion segments. Study 3: No differences existed in bilateral dynamic symmetry for the
        upper erector spinae; however, differences between groups did exist for the lower erector spinae.
        Conclusion: Repeatability of the EMG signal during quiet stance is acceptable; however, bilateral
        asymmetry may not be a definitive indicator of dysfunction. (J Manipulative Physiol Ther 2002;25:293-9)
        Key Indexing Terms: Electromyography; Erector Spinae Muscles; Low Back Pain
INTRODUCTION
         he use of the erector spinae electromyogram (EMG)          ers, a general consensus on the use of surface EMG in clinical
                                                                                                                                293
294   Lehman                                                                                  Journal of Manipulative and Physiological Therapeutics
      Clinical Use of PMG                                                                                                                 June 2002
         Study 1 addresses issues of between-day repeatability of      all influence measured EMG activity level. Nonhomogene-
      raw and normalized EMG signals during quiet standing.            ity in these factors between sides of the body may relegate
      Although well-researched, conflicting results have been          asymmetry in measured EMG activity to be the norm even
      shown. Dynamic tasks have shown moderate to high repeat-         though it is possible that bilateral muscles are contracting at
      ability,1,2,17 whereas evaluation of static tasks have demon-    equal intensities. Because of nonhomogeneity in the preced-
      strated poor repeatability4 or excellent repeatability,5 de-     ing factors we may be unable to adequately measure it.
      pending on the study. These inconsistencies in static tasks      Timing or activation profiles (linear envelope) of EMG
      motivated study 1; various normalization techniques were         activity is not influenced by these factors. One can compare
      employed in an attempt to improve the reproducibility of the     the shape of the EMG profile between bilateral muscle
      EMG signal during quiet stance across days.                      groups. In a small study (n ⫽ 6), Grabiner11 demonstrated
         The remaining 2 studies address the issue of asymmetry        differences in bilateral coupling of the EMG waveform in
      between bilateral erector spinae muscle groups during sym-       persons with LBP and control groups during isometric ex-
      metrical tasks. EMG asymmetry is often considered to be a        ertions at different loads. However, the statistical test used
      sign of dysfunction, although support for this belief is not     to assess asymmetry compared the phasic properties of the
      fully supported by the literature. Table 1 presents a brief      EMG signal with the amplitude characteristics; this may
      overview of the studies investigating EMG amplitude and          detract from the conclusion of the study based on the
      asymmetry differences between populations with LBP and           limitations in comparing amplitudes because of factors dis-
      pain-free controls. The studies appear to suggest that dif-      cussed earlier. It is possible to assess the phasic qualities of
      ferences exist between the groups during dynamic flexion         the EMG signal by using a simple cross-correlation func-
      tasks at peak flexion (ie, those with LBP typically lack the     tion.
      flexion relaxation phenomenon) and between the ratio of             In an attempt to explore all concepts of asymmetry,
      activity during forward flexion and re-extension. However,       studies 2 and 3 address 2 asymmetry concepts. Study 2
      EMG activity during other dynamic tasks and static tasks         explores whether a spinal segment that exhibits pain and
      does not appear to be statistically different between the 2      tenderness has more amplitude asymmetry than a segment
      groups. However, a general theme seems to be a trend for         within the same person who is free of pain and tenderness.
      increased activation in the group with LBP. The concept of       This study was motivated by the use of scanning EMG
      EMG amplitude symmetry between left and right erector            equipment that is often used to direct treatment of perceived
      spinae has also been investigated. Those who promote the         problematic segments because of their EMG asymmetry.
      use of scanning EMG suggest that left/right differences in       Study 3 evaluates the bilateral asymmetry of the erector
      EMG activation level are indicative of pathology and there-      spinae linear envelope during a dynamic forward flexion
      fore are suggestive of a biomechanical lesion. The research      movement using a cross-correlation function. This function
      to lend credence to this idea is mixed and sparse. Four large    only addresses issues of phasic imbalance but not amplitude
      studies4,6-8 have compared left/right EMG activity between       differences between the signals. The methods and results
      populations with LBP and populations without LBP during          will be presented together for each study followed by a
      static and dynamic tasks and demonstrated no differences         general discussion involving all 3 studies.
      between the 2 groups. Conversely, 2 smaller studies have
      shown contrary results. Aleksiev9 found differences in sym-      METHODS
      metry between groups with LBP and control groups during
      various levels of static contraction but no differences were        Three separate studies with different study protocols and
      found during rest. Similar results were found by Leach et        different subject populations were conducted. The follow-
      al10 in the lower erector spinae. Although the research on       ing sections will present the 3 different methods for each of
      asymmetry appears mixed, the more robust studies appear to       the separate experiments.
      indicate that amplitude asymmetry is not a distinguishing
      feature of low-back injured patients. However, none of           Study 1: Investigating Normalization
      these studies specifically directed the location of electrode       Patient characteristics. Eight subjects were recruited with no
      placement to the level of a spinal lesion (indicated by pain)    history of LBP within the past 6 months (5 men, 3 women;
      to adequately assess the idea that problematic segments are      age ⫽ 24.6 ⫾ 2.3 years, height ⫽ 175.5 ⫾ 10.3 cm, and
      inherently more asymmetrical than asymptomatic spinal            weight 73.2 kg ⫾ 12.15 kg). All read and signed informa-
      levels in controls or within the subject’s own spinal column.    tion and consent forms approved by the University of Wa-
         The reason the majority of studies to date have not           terloo Office of Research Ethics.
      demonstrated differences in symmetry between populations            Study protocol. The between-day repeatability of the average
      may be a result of many factors that modulate measured           EMG activity during quiet standing of the erector spinae
      EMG activity level that are not related to the level of neural   muscle at the L3 vertebrae was assessed on 3 different days.
      drive. Electrode placement, skin temperature, moisture, cu-      Day 1 and day 2 were 1 day apart, whereas day 3 was 6 days
      taneous fat distribution, and muscle-fiber type and size can     after day 2. During a single test session, bilateral EMG
Journal of Manipulative and Physiological Therapeutics                                                                                    Lehman   295
Volume 25, Number 5                                                                                                          Clinical Use of PMG
Table 1. Ability to discriminate populations based on EMG amplitude during static and dynamic tasks
 Kravitz, Moore, and            LBP ⫽ 22                 Evaluated EMG activity during       No differences between groups. Trends for
   Glavos15                     Control ⫽ 17               prone lying                         increased elevation in LBP
 Sherman8                       Control ⫽ 15             Tasks included sitting, standing,   No left/right asymmetry differences between
                                History of pain ⫽ 28       bending and rising.                 groups, no single aspect of EMG had
                                Experiencing pain ⫽ 83                                         predictive value.
                                                                                             Large variability in raw values.
                                                                                             Trends existed suggesting pain sufferers had
                                                                                               higher EMG levels.
 Miller16                       LBP ⫽ 11                 Performed sitting and standing      No differences in EMG amplitude between
                                Control ⫽ 11               trials                              groups
 Ahern et al.4                  LBP ⫽ 20                 Performed flexion/extension,        Static stance correctly classified 59% of subjects
                                Control ⫽ 20               rotation and stance                 with no difference found in EMG amplitude
                                                                                               or bilateral symmetry between groups.
                                                                                             Using lumbar ROM, EMG activity during peak
                                                                                               flexion, EMG activity during flexion correctly
                                                                                               classified 89% of subjects.
 Arena et al  19                Control ⫽ 29             Evaluated EMG levels during         Discriminant function analysis correctly
                                Spondyloarthritis ⫽ 19     sitting, standing, bending and      classified 52.4% of subjects.
                                Disk ⫽ 52                  rising in various populations       ANOVA analysis found no differences in
                                Nonspecific ⫽ 66           of LBP patients                     bilateral asymmetry between groups, controls
                                Combined ⫽ 17                                                  had less activity during stance than all other
                                Other ⫽ 24                                                     groups.
                                                                                             Different groups showed differences in EMG
                                                                                               activity levels depending on movement task.
 Sihvonen et al2                Controls ⫽ 25            Performed forward bending,          Did not quantify differences between groups
                                LBP ⫽ 87 (52 had no        extension and stance                during stance.
                                  pain during testing)                                       41% of all patients lacked FRP (31 total)
                                                                                             Only 10% of pain free showed no FRP.
                                                                                             Patients differed from controls in ratio of EMG
                                                                                               activity found during flexion and extension.
 Alexiev9                       LBP ⫽ 40                 EMG collected during static         No significant bilateral differences found at 0%
                                Control ⫽ 40              exertions of 50%, 30% and 0%         in either group.
                                                          of maximum voluntary               Significant differences in bilateral EMG at 30%,
                                                          contraction.                          50% & 100% MVC in LBP group but not in
                                                                                                controls.
 Leach, Owens, and              LBP ⫽ 10                 Collected paraspinal EMG            Significant differences between groups in ratio
   Giesen10                     non-LBP ⫽ 6                during, stance, forward             of thoracic ES activity and lumbar ES activity
                                                           flexion-extension                   and left/right asymmetry at lower ES.
                                                                                             Loss of FRP in LBP group
 Watson18                       Control ⫽ 2              Performed forward flexion and       No differences between groups during stance.
                                LBP ⫽ 70                   extension. Developed a            Patients had a significantly higher activity
                                                           flexion/relaxation ratio            during the peak flexion posture and
                                                           comparing peak activity during      significantly lower flexion/relaxation ratio.
                                                           flexion with that found during    Discriminant analysis revealed sensitivity of
                                                           maximally flexed position.          75% and sensitivity of 93%.
 Grabiner, Koh, and             LBP ⫽ 7                  EMG activity recorded during        Significant differences were found between
   Ghazawi11                    Control ⫽ 6               isometric exertion at 2 trunk        groups in bilateral coupling.
                                                          angles
  FRP, Flexion relaxation phenomenon; ES, erector spinae; ROM, range of motion.
296   Lehman                                                                                     Journal of Manipulative and Physiological Therapeutics
      Clinical Use of PMG                                                                                                                    June 2002
      activity was conducted during 5 trials of quiet standing.            whereas a transformed score of –1 indicates the left mus-
      Each quiet-standing trial lasted 5 seconds and each trial was        cular activity was twice as great as the right. After all
      preceded by 5 seconds of stepping forward and backward.              transformed scores were calculated, the absolute value of
         Disposable bipolar Ag-AgCl disc surface electrodes with           each score was used to find the average ratio for the group.
      a diameter of 1 cm were adhered bilaterally over the erector         To find the transformed score, the right erector spinae
      spinae musculature. Raw EMG was band-pass filtered (10               activity was first divided by the left erector spinae activity.
      and 500 Hz) and analogue-to-digital (A/D)– converted at              If the ratio was ⬎1, then 1 was subtracted from the ratio to
      1024 Hz. The signal was then full-wave rectified, and low-           give the transformed score. If the ratio was ⬍1, then the
      pass filtered (Butterworth filter cut-off frequency of 2.5Hz)        following formula was used: (1/ratio – 1) ⫻ (–1).
      to produce a linear envelope. The signals were then nor-
      malized to the amplitude obtained during the submaximal              Study 2: Asymmetry in Paraspinal EMG Amplitude During Quiet Stance
      reference task and the peak amplitude obtained during the               Patients. Seventeen subjects with back pain (14 with LBP,
      maximum voluntary contraction (MVC) tasks.                           3 with thoracic pain below T4) were referred from the
         Normalization tasks procedure. The different normalization pro-   University of Waterloo-Canadian Memorial Chiropractic
      cedures occurred on the same task session as the quiet-              College (UW-CMCC) Research Clinic. Nine subjects were
      standing trials. The MVC tasks occurred before the stance            male (height ⫽ 171 ⫾ 5 cm. weight ⫽ 73.5 ⫾ 8.04 kg, age
      trials, and the 4 trials of the submaximal task occurred after       ⫽ 26.6 ⫾ 13 years) and 8 subjects were female (height ⫽
      the tasks. The MVC required the subject to lie prone on a            164.25 ⫾ 7.5 cm, weight ⫽ 57.6 ⫾ 6.4 kg, age ⫽ 20.1 ⫾
      bench with his or her trunk over the ledge while the legs            1.5 years). All read and signed information and consent
      were strapped to the table. The subject was then required to         forms approved by the University of Waterloo Office of
      perform a maximum extension effort against the resistance            Research Ethics.
      of 1 or 2 experimenters. Two MVCs were performed with 3                 Task protocol. Subjects were examined by the clinic chiro-
      minutes of rest between each exertion. The maximum ac-               practor. A segment exhibiting pain and a therapist-per-
      tivity found was used as the reference amount. The sub-              ceived motion restriction was identified by manual palpa-
      maximal task required the subject to hold a 5-kg weight              tion. We recognized the concerns regarding the reliability of
      suspended from 45-cm chain and bar 1 cm off the floor                motion palpation; therefore pain and local tenderness were
      while maintaining a lordotic back with a slight bend at the          the deciding factor in determining the site for electrode
      knee and a greater bend at the hips in a standing position.          placement. Disposable bipolar Ag-AgCl disc surface elec-
      The EMG signals were processed in the same manner as                 trodes with a diameter of 1 cm were adhered bilaterally over
      those from the standing trials.                                      the erector spinae musculature at the painful segment level
         Normalization techniques. The raw data during stance was nor-     and at a nonpainful and nonrestricted segment, 5 segments
      malized using 3 different techniques. The data was first             superior or inferior to the painful segment. Typically, the
      expressed as a percent of the maximum activity found                 nonpainful segment was superior to the painful segment.
      during the maximum exertion (% MVC). The second nor-                 Only when the painful and restricted segment was above T7
      malization technique expressed the data as a percent of the          was a nonpainful segment located inferiorly (3 occurrenc-
      peak activity found during one submaximal reference task.            es). EMG signals were collected for 20 seconds during quiet
      The third normalization technique expressed the raw stance           standing 2 times and 4 minutes apart.
      data as a percent of average EMG activity during the four               EMG processing. Raw EMG was band-pass filtered (10 and
      submaximal tasks. It should be stressed that the same-day            500 Hz) and A/D converted at 1024 Hz. The amplifier had
      stance data was normalized to the same-day normalization             a CMRR of 10,000:1. The signal was then full-wave recti-
      task data.                                                           fied, and low-pass filtered (filter cut-off frequency of 2.5Hz)
         Data analysis. A 1-way random-effects model calculated the        to produce a linear envelope.
      single measure intraclass correlation coefficient (ICC) for             Statistical analysis. After the average activity of the linear
      the quiet-standing EMG values for the 4 normalization                envelope during quiet stance was calculated, a symmetry
      conditions: (1) raw, (2) percent MVC, (3) percent submaxi-           ratio could be calculated. The method for calculating the
      mal, and (4) percent average of the EMG average during               symmetry appears in the “methods section” for study 1.
      submaximal tasks. In addition, the repeatability of the sym-         After all transformed scores were calculated, the absolute
      metry between bilateral muscle groups was also assessed              value of each score was used to find the average ratio for the
      between days. The symmetry between bilateral muscle                  group. The absolute values of the symmetry ratios for the
      groups was quantified by first using a symmetry transform.           painful segment and for the nonpainful segment were then
      The transform allows the comparison of ratios between left           compared using a 1-way analysis of variance.
      and right muscle groups across persons when ratio values of
      ⬎1 or ⬍1 are produced. A transformed score of 0 indicates            Study 3: Asymmetry of Paraspinal EMG During Dynamic Tasks
      perfect symmetry. A transformed score of ⫹1 indicates the              Patient characteristics. The data analysed in this study had been
      right muscular activity was twice as great as the left,              previously collected in 2 separate previous studies. The first
Journal of Manipulative and Physiological Therapeutics                                                                             Lehman   297
Volume 25, Number 5                                                                                                   Clinical Use of PMG
study7 investigated lumbar kinematics and associated trunk             ence task, and 17.2% when normalized to the average value
muscle EMG in a healthy population. Data from 14 random                found during repeated submaximal reference tasks.
subjects from the study’s 24 subjects (17 men [age ⫽ 22 ⫾                 Asymmetry in muscle activity was present regardless of
3.4 years, height ⫽ 178.1 ⫾ 5.1 cm, and weight ⫽ 77 ⫾ 6.7              normalization procedure. On average, differences between
kg] and 7 women [age ⫽ 20.4 ⫾ 0.5 years, height ⫽ 166.1                the left and right side ranged from 65% to 74% (SD ⫽ 54%
⫾ 4.4 cm, and weight ⫽ 71 ⫾ 9.7 kg]) was assessed in the               to 60.9%; Tables 2 and 3). The ICCs for symmetry between
present study. The second study population was drawn from              the 2 sides showed less repeatability than the other variables
a previous study12 that examined trunk kinematics and                  measured (ICC ⫽ 0.43-0.773). Normalization to a maxi-
associated EMG in a convenience sample of persons with                 mum voluntary contraction did not improve the repeatabil-
chronic LBP drawn from the UW-CMCC Research Clinic.                    ity of symmetry scores relative to using raw EMG. How-
Data from 12 subjects (7 women and 5 men [age ⫽ 29.4 ⫾                 ever, the normalization procedures using submaximal ref-
3.05 years, height ⫽ 167.7 ⫾ 11.1 cm, and weight ⫽ 70.6                erence tasks improved repeatability relative to raw EMG
⫾ 13.6 kg]) was assessed. All read and signed information              values.
and consent forms approved by the University of Waterloo
Office of Research Ethics.                                             Study 2
    Task procedure. With feet shoulder width apart and knees              The mean absolute-transformed ratio score was .51 (SD
slightly bent, the subject flexed forward in the sagittal plane        ⫽ .36) for the segments exhibiting pain and .69 (SD ⫽ .64)
until full flexion was reached with the arms and head                  for the segment with no pain. There were no statistically
hanging freely. The subjects were instructed to pause for a            significant differences between the 2 segments of interest.
moment at full flexion, then rise to an upright posture. The
subjects performed this task 3 times.                                  Study 3
    EMG collection and processing. Raw EMG signals were collected         For the upper erector spinae, the mean cross-correlation
during the flexion extension tasks using disposable bipolar            coefficient healthy population was .86 (SD ⫽ .06), whereas
Ag-AgCl disc surface electrodes with a diameter of 1 cm                the coefficient for the group with LBP was .85 (SD ⫽ .07).
that were placed parallel to the muscle fibers with a center-          No significant difference was found between these two
to-center spacing of 3 cm over the following muscles bilat-            groups for this muscle study. However for the lower erector
erally: thoracic erector spinae (approximately 3-cm lateral            spinae, a statistically significant difference in cross-correla-
to T9 spinous process); lumbar erector spinae (approximate-            tion coefficients was found between groups. The population
ly 3-cm lateral to L3 spinous process). EMG signals were               without LBP had an average score of 0.93 (SD ⫽ 0.02),
sampled at 1024 Hz (Watscope A/D Convertor 12 bit,                     whereas the population with LBP averaged a score of 0.86
Northern Digital Inc, Waterloo, Ontario, Canada) and band-             (SD ⫽ 0.08).
pass filtered (10 and 500 Hz) for a total of 4 channels. The
amplifier had a common mode rejection ratio of 10,000:1.               DISCUSSION
The signals were then full-wave rectified and low-pass                    Normalization techniques did improve the repeatability
filtered (Butterworth filter cut-off frequency of 2.5 Hz).             of the EMG signal; however, all trials, normalized and
    Statistical analysis. A cross-correlation comparing the left and   non-normalized, demonstrated excellent repeatability of the
right erector spinae dynamic EMG profile (upper and lower)             EMG signal, with ICCs above 0.75. This suggests that
for the 3 flexion trials was used. The correlation numbers             normalization is not necessary to compare the results of 1
produced for the populations with and without with LBP                 person with himself over time for quiet-stance trials. How-
were assessed for differences using a 1-way analysis of                ever, without normalization it is still difficult to compare
variance.                                                              across persons and to allow for a biologically relevant
                                                                       interpretation of the EMG signal as a result of the various
                                                                       factors, other than muscle activation, that modulate EMG
RESULTS                                                                signal amplitude. A large between-subject variability in
Study 1                                                                EMG amplitude has been demonstrated in previous studies,8
   Repeatability was acceptable regardless of the normaliza-           as has the risk of non-normalization in proper biologic
tion procedure. Each normalization improved the repeat-                interpretation of EMG signals.12 An interesting observation
ability of the measured EMG signal relative to unnormal-               was the variability of the EMG signal about the mean during
ized data. It should also be noted that although repeatability         within-day trials. This suggests the importance of conduct-
was deemed statistically acceptable, within- and between-              ing multiple trials to average the signal across trials. This
variability still existed. The average standard deviation of           variablility is most likely a result of the relatively low
EMG activity across all days expressed as a percentage of              activity during stance and the way in which this activity can
the mean was 17.3% for raw EMG, 20.9% when normalized                  be easily influenced by small changes in posture and sub-
to MVC, 17.8% when normalized to a submaximal refer-                   sequent stability demands on the erector spinae. Subjects
298   Lehman                                                                                      Journal of Manipulative and Physiological Therapeutics
      Clinical Use of PMG                                                                                                                     June 2002
      Table 2. ICC scores for erectors spinae activity during quiet         Table 3. Average Symmetry score across the population on all
      stance                                                                three different experiment days
Normalization Technique Right ES Left ES Normalization Technique Asymmetry Score and ICC
       None raw amplitude                     0.78                 0.87       None raw amplitude                           .65 (.609) ICC ⫽ .59
       % MVC                                  0.88                 0.926      % MVC                                        .66 (.54) ICC ⫽ .43
       % submaximal MVC                       0.82                 0.925      % submaximal VC                              .74 (.56) ICC ⫽ .67
       % average submax MVC                   0.84                 .93        % average submaximal VC                      .67 (.54) ICC ⫽ .773
        ES, Erector spinae; MVC, maximum voluntary contraction.                ICC, Intraclass correlation coefficient; MVC, maximum voluntary con-
                                                                            traction; VC, voluntary contraction.
         rhythm in low-back pain patients and healthy controls.               bilateral paraspinal excitation in subjects with low-back
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