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. Author manuscript; available in PMC: 2020 Oct 1.
Published in final edited form as: Clin Biomech (Bristol). 2019 Jul 5;69:104–108. doi: 10.1016/j.clinbiomech.2019.07.007

Muscle activation during maximum voluntary contraction and m-wave related in healthy but not in injured conditions: Implications when normalizing electromyography

Jennifer A Zellers a, Sheridan Parker b,c, Adam Marmon a, Karin Grävare Silbernagel a
PMCID: PMC6823141  NIHMSID: NIHMS1535129  PMID: 31326725

Abstract

Background:

Electromyography signal amplitude is influenced by a variety of factors. Normalization strategies aimed at decreasing signal variability include using peak electromyography signal during a maximum voluntary contraction and peak-to-peak M-wave amplitude. However, whether these normalization methods are comparable has not been investigated in injured populations. This study investigated the relationship between peak signal during maximum voluntary contraction and M-wave amplitude in individuals with a unilateral Achilles tendon rupture. Secondarily, we observed whether the two normalizations strategies would yield similar results when evaluating between limb differences in muscle activity during a jump task.

Methods:

Eleven individuals 1-3 years after a unilateral Achilles tendon rupture were included in this study. Surface electromyography was used on the medial and lateral gastrocnemii bilaterally. Peak maximum voluntary contraction, M-wave amplitude, and electromyography during a jumping task were collected.

Findings:

A strong relationship was observed between peak maximum voluntary contraction and M-wave amplitude on the uninjured (r=0.71-0.88, P < 0.05) but not on the ruptured side (r=0.41-44, P > 0.05). The two normalization techniques did not produce different results when comparing the uninjured and ruptured sides.

Interpretation:

The findings of this study suggest that M-wave normalization yields similar results as peak maximum voluntary contraction-normalized electromyography in uninjured conditions. M-wave normalization may be a useful strategy in an injured population where a maximal muscle contraction is unsafe or impaired.

Keywords: Achilles, rupture, muscle, recruitment, inhibition

1. Introduction

Electromyography (EMG) is a technique used to assess muscle activation. EMG signal amplitude is influenced by a variety of factors, is highly variable between individuals, and typically requires normalization for between subject or across session comparisons (Cronin et al., 2015). A variety of normalization factors have been proposed – such as peak activity during a dynamic task (Suydam et al., 2016), maximum voluntary contraction (MVC), and artificial stimulation (e.g. M-wave) (Buckthorpe et al., 2012; Cronin et al., 2015). All of these strategies have been used to standardize inter-subject and intra-session variability for comparison (Buckthorpe et al., 2012; Cronin et al., 2015; Suydam et al., 2016), however, there is no consensus regarding which technique is optimal and selection of the ideal technique is likely context dependent (Ball and Scurr, 2013).

EMG signal is often normalized to an individual’s MVC – or the peak EMG during a task yielding the theoretical maximum amplitude of activation during a muscle contraction, but there are a variety of concerns when using this normalization strategy. Normalizing to an MVC is commonly used in healthy individuals, but may present with limitations or not be possible in injured populations. In some pathological conditions, maximal contraction of a muscle may not be safe in the early phases of healing. In addition to safety concerns, an inability to fully activate the muscle has been found to interfere with obtaining an accurate representation of the muscle recruitment capacity, referred to as an activation deficit (Chmielewski et al., 2004; Manal and Snyder-Mackler, 2000; Mizner et al., 2003; Palmieri-Smith et al., 2009). In the context of EMG normalization, this raises concerns that differences in activation deficit may skew the interpretation of findings when comparing normalized EMG signal between limbs or to a control group.

Additionally, from a conceptual standpoint peak MVC represents the maximum amplitude of electrical activity within a muscle. When using the peak MVC to normalize a ballistic contraction, however, is it not uncommon for the muscle activity observed during the ballistic task to exceed that of the MVC (Suydam et al., 2016). This presents a challenge in interpreting this result from a physiological standpoint.

M-wave normalization is a non-volitional technique that has been used to normalize EMG signal (Buckthorpe et al., 2012; Cronin et al., 2015) and has been suggested to potentially overcome some of the concerns of MVC normalization (Buckthorpe et al., 2012). This technique involves standardizing EMG amplitude during a dynamic task to a compound muscle activation potential, which equates to maximum motor neuron recruitment. Pragmatically, this involves providing transcutaneous electrical stimulus to a superficial nerve and increasing the stimulus until muscle recruitment plateaus, visualized as the M-wave reaching its peak amplitude. One metric that can be used for normalization is the maximum peak-to-peak M-wave amplitude, or Mmax (Buckthorpe et al., 2012). M-wave normalization has been previously used to normalize EMG in a population of individuals after Achilles tendon rupture (Wang et al., 2013), however, the relationship between peak MVC and Mmax has not been compared in injured populations.

Use of a non-volitional normalization strategy such as M-wave normalization may be particularly helpful in exploring muscle activity in individuals with Achilles tendon rupture. Clinically, activation of the triceps surae musculature is of great concern in this population as it appears that calf muscle function does not fully recover following injury even in the long-term (Brorsson et al., 2017; Heikkinen et al., 2016; Lantto et al., 2015). Prior work has identified anatomical deficits of the gastrocnemius and soleus, such as muscle atrophy (J Heikkinen et al., 2017; Juuso Heikkinen et al., 2017; Rosso et al., 2013), reduction in fascicle length (Peng et al., 2017), fatty infiltration of the muscle (Juuso Heikkinen et al., 2017), and alterations in muscle recruitment in the affected triceps surae (Wang et al., 2013). This population could be ideal to investigate the relationship between peak MVC and Mmax due to the ease of stimulating the tibial nerve along with the potential benefit of having a normalization strategy that could be used relatively early in patient recovery.

Therefore, the aim of this study was to investigate the relationship between Mmax and peak MVC normalized EMG during a counter movement jump (CMJ) in a group of individuals with a unilateral Achilles tendon rupture. We hypothesized that in a healthy limb (the uninjured side) peak MVC and Mmax would be strongly related. However, in the presence of pathology, such as an Achilles tendon rupture, peak MVC and Mmax would show a weaker relationship. We further hypothesized that peak MVC and Mmax would capture similar amounts of variability (deviation from the mean), which would be an important consideration when selecting a normalization strategy. Secondarily, we sought to determine if the two normalizations strategies would yield similar outcomes when evaluating muscle activity during a jump task in a group of individuals with Achilles tendon rupture. We were interested whether or not a hypothetical study using an MVC versus and Mmax would yield different interpretations. To investigate this, we compared the ruptured to uninjured side gastrocnemius activity during the CMJ to see if one normalization technique would result in significant side-to-side differences where the other did not.

2. Methods

Individuals 1-3 years following unilateral Achilles tendon rupture with repair were included in this study. Participants were excluded if they had a history of seizures or epilepsy, pacemaker or implanted cardiac defibrillator, implanted nerve stimulator, peripheral neuropathy, or were pregnant. Participants were also excluded if they had bilateral rupture, significant postoperative complication such as deep wound infection, an augmented repair/reconstruction, or were unable to comfortably and painlessly perform a unilateral jump task. The study was approved by University of Delaware Institutional Review Board, and all participants were instructed about the study protocol and consent was obtained prior to inclusion.

Participants completed a single study session in which they filled out questionnaires, were fitted with surface electrodes, underwent MVC and M-wave assessment, and performed a jump task in a motion capture laboratory. All testing procedures were performed on the right followed by left lower extremities to randomize the order of injured versus non-injured limbs in the rupture cohort.

For descriptive purposes, all participants completed a physical activity scale(Grimby, 1986). This is a 6-point scale with higher scores indicating higher levels of physical activity. Participants also completed the Achilles tendon Total Rupture Score(Nilsson-Helander et al., 2007), which is a self-reported outcome measure. This is a 100-point scale with higher scores indicating lower levels of symptoms and higher levels of function.

2.1. Mmax and Peak MVC Data Collection

Surface EMG electrodes were placed on the medial and lateral gastrocnemii according to SENIAM guidelines (Hermens et al., 2000; Hermens and Freriks, n.d.) with a reference electrode at C7. The skin was shaved and abraded with isopropyl alcohol. Electrodes were secured with tape and elastic bandages. Electrodes were wired, double differential, 12 mm diameter electrodes with a 17 mm inter-electrode distance and 20x preamplification at the pick-up site (MA300 EMG System, Motion Lab Systems, Baton Rouge, LA, USA).

Participants were asked to lie prone while a stimulating electrode was applied to the back of the knee over the posterior tibial nerve at an area that evoked the largest motor response. A single-pulse l00μs duration, monophasic stimulus was increased in amplitude until the compound muscle action potential plateaued, when the M-wave reached peak amplitude and no longer increased with increasing stimulation. The stimulation was then increased by 10% to ensure a suprathreshold stimulus. Three pulses of the suprathreshold stimulus delivered at least 10 seconds apart were recorded and the peak-to-peak M-wave amplitude, averaged across the three trials, was used for normalization. EMG signal during the M-wave was collected at 5,000 Hz, using Signal software (Cambridge Electronic Design Limited, Cambridge, UK).

MVC data were collected at 1080 Hz using Nexus software (Vicon Motion Systems Ltd, Oxford, UK). Plantar flexion MVC was performed while standing, with the participant utilizing two fingers on a table for balance. Participants were asked to do a bilateral heel rise, “squeezing your calves as hard as you can.” Strong verbal encouragement was provided. This task was selected for MVC assessment as an isometric contraction in a standardized ankle angle may not yield similar force or muscle activity on the ruptured relative to the uninjured side. We also selected this task because it uses similar ankle range of motion as is used in the CMJ.

2.2. Functional Testing

The functional test used to compare normalization strategies was a unilateral CMJ. Participants were instructed to place their hands across their chest and jump as high as possible, trying to take off and land in the same place. Three repetitions were performed on each leg and legs were alternated on consecutive trials.

Kinematic and kinetic data were used to synchronize EMG signal to the CMJ. Thirty-nine retroreflective markers were placed on the pelvis and lower extremities(Di Stasi et al., 2012), and marker data was collected at 120 Hz using an 8-camera system (Vicon Motion Systems Ltd, Oxford, UK). Kinetic data was collected using two, in-ground force plates (Bertec Corporation, Columbus, OH, USA) at a sampling rate of 1080 Hz. EMG data was collected at a sampling rate of 1080 Hz.

2.3. EMG Processing

EMG and motion capture data were processed using Visual 3D software (C-Motion, Inc., Germantown, MD, USA) using a custom written script to automate processing. EMG signals from the MVC and CMJ trials were filtered using a 30-350 Hz bandpass 4th order Butterworth filter. The signal was then processed with a 100 ms root mean squared window. The peak MVC signal was used to normalize the EMG signal from CMJ trials. Because the M-wave is a short duration signal with very little noise, peak-to-peak amplitude was calculated from an unfiltered signal and used to normalize the CMJ trials.

For the CMJ, the takeoff phase was defined as the period from peak knee flexion (identified with kinematic data) to take off (when the foot left the force plate) and served as the period of interest. EMG signals were integrated from 250 ms prior to peak knee flexion through the end of take off to account for electromechanical delay. The average integrated signal of three trials was included in data analysis. Peak EMG amplitude was identified by taking the signal maximum during this same time interval. The mean of three trials was included in data analysis.

2.4. Statistical Analysis

Descriptive statistics (means and standard deviations) were used to report collected measures. Pearson correlation analysis was performed to determine the relationship between peak MVC with Mmax. Data were examined to ensure the assumptions of parametric statistical testing were met and to identify any outliers (defined as a value greater than 3 standard deviations from the mean). Strength of relationships were interpreted as weak (r = 0.3-0.5), moderate (r = 0.5-0.7), and strong (r > 0.7)(Hinkle DE, Wiersma W, 2003).

Coefficient of variation was calculated for each normalization strategy, and is reported descriptively. In order to determine whether or not peak MVC or Mmax captured greater variability relative to the population mean, Levene’s test for homogeneity of adjusted coefficient of variation scores was performed to compare homogeneity of peak MVC versus Mmax in ruptured and uninjured sides and in both muscles of interest.

A paired t-test was used to identify whether there were differences in peak, normalized EMG in the ruptured compared to the uninjured side. Cohen’s d was calculated to estimate effect size for between limb comparisons.

3. Results

Eleven participants (10 male, 1 female) with a mean(SD) age of 44(9) years and BMI of 25.9(3.2) kg/m2 were included in this study. Participants scored 5.0(1.4) out of 6 possible points on the physical activity scale and 82(15) out of 100 possible points on the Achilles tendon Total Rupture Score.

The relationships between peak MVC and Mmax in all conditions and muscles are displayed in Figure 1. Strong, significant relationships were observed between MVC and Mmax on the uninjured side (r = 0.71-0.88, P ≤ 0.02), whereas, weak, non-significant relationships were observed on the ruptured side (r = 0.41-0.44, P > 0.15).

Figure 1.

Figure 1

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Relationship between raw peak maximum voluntary contraction and M-wave peak-to-peak amplitude.

There were no significant differences in homogeneity of the adjusted coefficient of variation scores between normalization techniques (P = 0.19-0.82). The coefficient of variation for raw peak MVC ranged from 31.2-41.7% across muscles and ruptured/uninjured conditions. The coefficient of variation for raw Mmax ranged from 39.2-56.% across muscles and ruptured/uninjured conditions.

No significant side-to-side differences in peak EMG were observed between limbs using either normalization strategy. The results for the paired t-test comparing side-to-side differences in peak, normalized EMG during a counter movement jump is displayed in Table 1.

Table 1.

Mean(SD) of Peak EMG Signal Normalized by Different Strategies During the Takeoff Phase of a Counter Movement Jump.

Muscle Normalization
Strategy		 Ruptured
Side		 Uninjured
Side		 P-value Cohen’s d
Lateral Gastrocnemius MVC 1.45(0.60) 1.22(0.34) 0.16 0.47
Mmax 0.078(0.040) 0.064(0.028) 0.32 0.41
Medial Gastrocnemius MVC 1.45(0.57) 1.26(0.43) 0.49 0.38
Mmax 0.082(0.033) 0.083(0.055) 0.97 0.02
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P-value and effect size (Cohen’s d) are for between side comparisons. MVC – maximum voluntary contraction, Mmax – M-wave peak-to-peak amplitude.

4. Discussion

This is the first study to compare M-wave peak-to-peak with MVC EMG normalization strategies in individuals with tendon injury. As hypothesized, we found that there were strong relationships between raw peak MVC and Mmax values on the uninjured side, however, these relationships deteriorate in the presence of pathology. Both techniques showed similar amounts of variability. Taken together, these findings suggest that either peak MVC or Mmax could be used in the normalization of EMG from healthy individuals, however, it may be beneficial to use Mmax in populations where the ability to volitionally contract a muscle is impaired. Despite weaker relationships between normalization strategies in the presence of pathology, results of between limb comparisons in peak EMG were similar with both peak MVC and Mmax normalization in well-recovered individuals. This suggests that Mmax could be a good alternative for EMG normalization in cases where an MVC is unsafe or impaired.

There are a variety of pros and cons with both MVC and M-wave normalization techniques. MVC has been commonly used (Ball and Scurr, 2013) and has been found to be reliable over time in healthy individuals (Ball and Scurr, 2010; Buckthorpe et al., 2012), however, may have limitations as volitional muscle activation has been found to be impaired following injury (Mizner et al., 2005, 2003; Snyder-Mackler et al., 1994; Stevens et al., 2003). We observed a deterioration of relationship between MVC and Mmax with pathology, however, the two normalization strategies yielded similar results when comparing side-to-side differences in peak normalized EMG amplitude within this particular group of individuals who had recovered well after Achilles tendon repair. M-wave overcomes concerns regarding muscle impairment since it is non-volitional and has the advantage of generating independent values for each muscle innervated by a given nerve. Our findings along with the non-volitional nature of M-wave normalization could indicate a benefit to using M-wave normalization in patients where an MVC is unsafe or where there is concern that volitional muscle activity could be impaired.

In the context of tendon injury, it is not safe to perform MVCs in the first several weeks of healing due to the loads placed on the tendon. There were no adverse events when collecting M-wave maximum peak-to-peak amplitude, and this was able to be collected simultaneously at the medial/lateral gastrocnemii. Some individuals did report discomfort at the site where the stimulus was delivered during testing, but discomfort stopped upon completion of M-wave collection and there were no other participant complaints (no tendon-related discomfort, etc.). This study did not investigate the use of M-wave early after Achilles tendon rupture, but peak strain and time under tension in the tendon with a twitch response would be lower than with an MVC particularly if the foot is positioned in plantar flexion when the stimulus is delivered. Additionally, the foot does not encounter any resistance when collecting EMG data during an M-wave, making it a more viable option early in recovery from tendon injury. M-wave does require special equipment, time to collect data, and anatomical considerations (requires a superficial nerve location to stimulate) that limits its utility.

This study was limited by small subject numbers in a predominantly male group, which may underestimate the strength and statistical significance of the relationships observed. Additionally, as this was a small, preliminary study we did not adjust for multiple comparisons in the t-test portion of the study. The individuals with Achilles tendon rupture recruited for this study had recovered very well, evidenced by high ATRS and PAS scores and need to fulfill inclusion/exclusion criteria of being able to jump on one leg, which may underestimate differences between limbs. Despite these limitations, this study is the first to compare peak MVC and Mmax normalized EMG during a dynamic task (CMJ) in individuals with tendon injury. Furthermore, it supports the use of Mmax normalization as a comparable alternative to peak MVC normalization in uninjured conditions, along with potential benefits when working with injured populations where muscle inhibition is of concern or in cases where individual muscle contributions are of particular interest.

5. Conclusions

In the absence of injury, raw peak MVC and Mmax values are strongly related. In the context of Achilles tendon rupture, however, these relationships diminish. These relationships suggest that Mmax could be a good alternative to an MVC where volitional contraction is impaired or unsafe. When normalizing EMG, either peak MVC or Mmax can be used in the study of healthy individuals, but normalizing to the Mmax may be preferable in injured individuals where the muscle of interest is innervated by a superficial nerve.

Highlights.

  • Normalizing electromyography in individuals with muscle inhibition is challenging

  • M-wave normalization may be useful but has mostly been studied in healthy normals

  • We measured maximum voluntary contraction and M-wave in people with Achilles repair

  • Maximum voluntary contraction and M-wave were related only on the uninjured side

  • M-wave is preferable to normalize electromyography in populations with concern for inhibition

Acknowledgments

Funding: This work was supported by the National Institute of Arthritis and Musculoskeletal and Skin Diseases of the National Institutes of Health under Award Number R21AR067390. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. This research was also supported by the Foundation for Physical Therapy and the University of Delaware Research Foundation. The funding sources for this study had no role in the study design, collection, analysis, interpretation of data, writing, or submission of this manuscript.

Footnotes

Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

Declaration of interest: The authors report grant funding from the National Institutes of Health, Foundation for Physical Therapy, and University of Delaware Research Foundation for this study, but have no additional conflicts of interest.

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