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Assessing the validity of surface electromyography for recording muscle activation patterns from serratus anterior
Journal of Electromyography and Kinesiology 24 (2014) 221–227
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Journal of Electromyography and Kinesiology journal homepage: www.elsevier.com/locate/jelekin
Assessing the validity of surface electromyography for recording muscle activation patterns from serratus anterior Lucien Hackett a, Darren Reed b,⇑, Mark Halaki a, Karen A. Ginn b a b
Discipline of Exercise and Sport Science, Faculty of Health Sciences, The University of Sydney, Australia Discipline of Biomedical Science, Sydney Medical School, The University of Sydney, Australia
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Article history: Received 27 June 2013 Received in revised form 10 January 2014 Accepted 17 January 2014
Keywords: Shoulder Serratus anterior Muscle activation Electromyography
a b s t r a c t Purpose: No direct evidence exists to support the validity of using surface electrodes to record muscle activity from serratus anterior, an important and commonly investigated shoulder muscle. The aims of this study were to determine the validity of examining muscle activation patterns in serratus anterior using surface electromyography and to determine whether intramuscular electromyography is representative of serratus anterior muscle activity. Methods: Seven asymptomatic subjects performed dynamic and isometric shoulder flexion, extension, abduction, adduction and dynamic bench press plus tests. Surface electrodes were placed over serratus anterior and around intramuscular electrodes in serratus anterior. Load was ramped during isometric tests from 0% to 100% maximum load and dynamic tests were performed at 70% maximum load. EMG signals were normalised using five standard maximum voluntary contraction tests. Results: Surface electrodes significantly underestimated serratus anterior muscle activity compared with the intramuscular electrodes during dynamic flexion, dynamic abduction, isometric flexion, isometric abduction and bench press plus tests. All other test conditions showed no significant differences including the flexion normalisation test where maximum activation was recorded from both electrode types. Low correlation between signals was recorded using surface and intramuscular electrodes during concentric phases of dynamic abduction and flexion. Conclusions: It is not valid to use surface electromyography to assess muscle activation levels in serratus anterior during isometric exercises where the electrodes are not placed at the angle of testing and dynamic exercises. Intramuscular electrodes are as representative of the serratus anterior muscle activity as surface electrodes. Ó 2014 Elsevier Ltd. All rights reserved.
1. Introduction Electromyography (EMG) is the most reliable tool that researchers have to understand the complex activation patterns of muscles during exercises and functional activities (Basmajian and De Luca, 1985). EMG can be recorded by intramuscular electrodes placed into the belly of the muscle or surface electrodes placed on the overlying skin. Traditionally surface electrodes have been preferred for superficial muscles as they are non-invasive, easier to set up (Giroux and Lamontagne, 1989) and sample from a larger cross-section of the muscle than intramuscular electrodes (Basmajian and De Luca, 1985). However, surface electrodes may be susceptible to geometric ⇑ Corresponding author. Address: Discipline of Biomedical Science, Sydney Medical School, Cumberland Campus C42, The University of Sydney, Lidcombe, NSW 1825, Australia. Tel.: +61 2 9351 9144; fax: +61 2 9351 9715. E-mail address: [email protected] (D. Reed). http://dx.doi.org/10.1016/j.jelekin.2014.01.007 1050-6411/Ó 2014 Elsevier Ltd. All rights reserved.
displacement away from the target muscle (Oberg et al., 1992) and recording EMG signals from adjacent or underlying muscles, leading to contamination of signals, known as crosstalk (Johnson et al., 2011; Perry et al., 1981; Stokes et al., 2003). Intramuscular electrodes are commonly used to record activity from deep muscles inaccessible to surface electrodes, but may also be the electrode of choice in some superficial muscles if cross talk or geometric displacement is a potential problem. They record activity from a smaller volume of muscle having more specificity than surface electrodes and therefore, are not susceptible to crosstalk (Basmajian and De Luca, 1985; Bouisset and Maton, 1972; Giroux and Lamontagne, 1989). However, studies suggest that they may not be representative of activity in the entire muscle (Giroux and Lamontagne, 1989; Yemm, 1977). The shoulder region, with the humerus and scapula both moving through large ranges and multiple muscles with varying morphology lying in close proximity to each other, presents challenges in using surface electrodes on superficial shoulder muscles.
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Previous research in the shoulder region has shown geometric displacement (Oberg et al., 1992) and crosstalk from adjacent muscles in isometric (Johnson et al., 2011; Waite et al., 2010) and dynamic exercises (Jaggi et al., 2009) may lead to invalid recordings from surface electrodes. Serratus anterior is an important axioscapular muscle crucial to normal shoulder function. This large, flat muscular sheet attaches via individual digitations from the first 8 or 9 ribs to the medial border of the scapula (Palastanga et al., 2012). It is a major protractor of the scapula and the lower fibres co-ordinate with trapezius to upwardly rotate the scapula (Palastanga et al., 2012). EMG research investigating serratus anterior activity has predominantly used surface electromyography over the lower digitations of the muscle where it is most accessible and superficial (Cools et al., 2007; Decker et al., 1999; Ekstrom et al., 2003). However, glenohumeral joint movement results in the skin overlying the lower fibres of serratus anterior experiencing large degrees of shift during shoulder movement. There is also the possibility that surface electrode recordings from serratus anterior may be contaminated by potential cross-talk from adjacent muscles. To date, no studies have assessed the validity of using surface electrodes to record activity from serratus anterior. In addition, the issue of whether recording serratus anterior activity using intramuscular electrodes is representative of activity in the whole of this large muscle has not been investigated and is still unknown. Therefore, the aims of this experiment were to: Determine the validity of using surface electrodes to record muscle activity from the lower fibres of serratus anterior during dynamic and isometric contractions. In the test conditions where the validity of surface electrode recordings were confirmed, to determine the representativeness of intramuscular electrodes compared to surface electrodes for recording muscle activity from the lower fibres of serratus anterior. 2. Methods 2.1. Subjects Seven asymptomatic subjects (six male, one female, aged 19– 23) volunteered to participate in this investigation. To be eligible to participate subjects must have had no pain in their dominant shoulder in the previous two years and had never been treated for shoulder pain. Prior to the experiment, shoulder strength and range of motion tests were conducted by an experienced physiotherapist to verify normal pain free functioning of the dominant shoulder and subjects gave their informed consent. Ethics approval was granted by The University of Sydney’s Human Research Ethics Committee (approval number 04-2011/13610). 2.2. Instrumentation Electromyographic data were collected simultaneously from the lower fibres of serratus anterior using both surface and intramuscular electrodes. Intramuscular electrodes were manufactured in the Shoulder Laboratory, Sydney Medical School, using the technique developed by Basmajian and De Luca (1985) and comprised of two insulated wires of 0.14 mm diameter made of Teflon coated stainless steel. The two wires were bent back to form barbs at 2 mm and 4 mm respectively from the terminal end. This terminal end was de-insulated for a length of 1 mm for both wires. Using a sterile technique, the wires were inserted via a hypodermic needle acting as a cannula into the digitation of serratus anterior over rib 7 (Geiringer, 1994). Wires were looped to allow for adequate movement, and then taped to the skin to prevent inadvertent removal.
A pair of 3.2 mm diameter silver/sliver chloride surface electrodes (Red Dot, 2258, 3M, Sydney, Australia) was used to detect muscle activity from serratus anterior (Ekstrom et al., 2004). With the subject side-lying and the arm in 60° abduction, the surface electrodes for serratus anterior were placed at a distance of approximately 25 mm apart over the seventh rib (Ekstrom et al., 2005; Hardwick et al., 2006), in line with the muscle fibres and around the intramuscular electrodes (Giroux and Lamontagne, 1989; Johnson et al., 2011). A large ground electrode (Universal Electrosurgical Pad: Split, 9160F, 3M, Sydney, Australia) was placed on the spine and acromion of the contralateral scapula. Resistances were measured between surface electrodes (Dick Smith Electronics Q-1450) and were <5 kX. Both the intramuscular and surface electrodes were then connected to amplifiers (Iso-DAM8-8 amplifiers, World Precision Instruments, Sarasota, FL; gain = 100) via a junction box. Data was recorded on a personal computer using SPIKE 2 software (Version 4.0 Cambridge Electronics Design, Cambridge, UK) and a 16 channel analogue to digital converter (CED2701, CED Ltd., Cambridge, UK) at a sample rate of 3125 Hz. Maximum voluntary contractions (MVCs) were then performed using five standardised shoulder normalisation tests (Boettcher et al., 2008; Ginn et al., 2011) known to have a high likelihood of producing maximum activity in serratus anterior. These normalisation tests were performed in random order and consisted of manually resisted shoulder flexion with the shoulder at 125° flexion, internal rotation at 90° shoulder abduction, shoulder extension at 30° abduction, abduction with the shoulder abducted 90° and internally rotated and self-resisted horizontal adduction at 90° shoulder flexion. 2.3. Test positions Isometric and dynamic tests of shoulder flexion, extension, abduction, adduction and a dynamic bench press plus exercise (seated chest press to a point where the elbows are fully extended, followed by shoulder protraction) were performed. These tests were selected as they include tasks expected to elicit high serratus anterior activity (flexion and abduction, bench press plus) (Decker et al., 1999; Ludewig et al., 2004), as well as ones in which it would be expected to be less active (extension, adduction). The order of the isometric and dynamic tests was block randomised. During the abduction, adduction, flexion and extension tests the subject stood with their feet placed shoulder width apart and their contralateral hand placed on the corresponding hip in order to prevent unwanted trunk movement. For the flexion test, the contralateral foot was brought two feet-lengths forward, and for the extension test, the ipsilateral foot was brought two feet-lengths forward. The bench press plus exercise was performed on gym equipment (Hyper Extension Gym 50036, 150lbs). Prior to testing and electrode placement, the maximum isometric load (100% load) for shoulder abduction, flexion, adduction, and extension was measured using a load cell (XTRAN load cell S1W, Applied Measurement Australia PTY LTD, Melbourne, Australia), with resistance maintained for three seconds. Maximum tests were repeated twice, with at least a 30 s rest in between each repetition. The maximum load was used as the ramped isometric target load, and to calculate the 70% maximum load used during dynamic testing. The one repetition maximum (1RM) for the dynamic bench press plus exercise was calculated by the Bryzcki equation, using the number of repetitions a subject was able to perform sub-maximally to determine their 1RM (Bryzcki, 1995). The testing order of these maximal load tests was randomised. Dynamic tests included shoulder flexion, extension, abduction, adduction and bench press plus. The bench press plus, was performed seated and through range from 20° shoulder extension to 90° shoulder flexion, followed by full range scapular protraction
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F
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E i) Fig. 1. Performance of flexion (A), extension (B), abduction (C), adduction (D), bench press plus (E) during both dynamic (i) and isometric (ii) conditions. Force transducer (F).
(Fig. 1E). The other four shoulder movements were performed using a cable apparatus attached to a pulley (Fig. 1A–D). Abduction was performed from 0° to 160°, adduction from 140° to 0°, flexion from 30° extension to 160° flexion and extension from 140° flexion to 30° extension. Load was set at 70% of maximum load during these dynamic tests in order to produce a high level of muscle activity while avoiding the level of fatigue that comes with prolonged maximal exercise. Timing was monitored and standardised at three seconds during the concentric phase and three seconds during the eccentric phase of the exercises, with a one second pause between concentric and eccentric phases. The same body and foot positioning as
described above was monitored in order to ensure correct scapulohumeral rhythm during the execution of each test without compensatory trunk movement. A draw-wire was used (Microepsilon, 94496, Ortenburg, Germany) to synchronise shoulder movement with the EMG signals. Two repetitions of each dynamic test were performed in random order, with a 30 s rest interval between each repetition. Ramped isometric tests for shoulder flexion, extension, abduction, and adduction were performed randomly with at least 2 min rest between each test to avoid the effects of fatigue. Ramped exercises allowed for an examination of the effect of different isometric loads ranging from 0% to 100% of maximum
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load. Posture and feet positioning was monitored and standardised as in the dynamic tests. Using the load cell (XTRAN load cell S1W, Applied Measurement Australia PTY LTD, Melbourne, Australia) connected to an amplifier (DA100 BIOPAC Systems Inc, Goleta, CA USA) connected to an analogue to digital converter (MP100, BIOPAC Systems Inc, Goleta, CA, USA) and the AcqKnowledge Software (Version 3.9.0, BIOPAC Systems Inc, Goleta, CA, USA), subjects’ applied force and target force signals were displayed on a laptop computer. The ramped target signal consisted of a four seconds linear increase in force from zero to maximum, three seconds at maximum, then four seconds linear decrease back to zero (Fig. 2). Subjects were instructed to follow the target signal by applying the appropriate force level. Isometric tests were performed in standing using the same pulley apparatus as for the majority of the dynamic shoulder tests. The shoulder was positioned in 90° flexion in the sagittal plane for the flexion and extension tests and in 90° abduction in the scapular plane for the abduction and adduction tests. The isometric tests were performed twice in random order, with a 30 s rest interval between repetitions.
2.4. Data analysis Data processing was performed in Matlab (version 7, The Math Works, Natick, MA). EMG signals were high pass filtered at 10 Hz (zero lag, 8th Order Butterworth), notch filtered at 50 Hz (zero lag, 8th Order Butterworth), rectified then the linear envelope calculated by low pass filtering at 3 Hz (zero lag, 8th Order Butterworth). The EMG signals were then normalised using the maximum value recorded for the muscle during the five normalisation tests and expressed as (%MVC) separately for each of the surface and indwelling electrodes. The mean activation level from the lower fibres of serratus anterior as measured by the mean linear envelope of the EMG recorded using each type of electrode across each trial of each isometric test was calculated as well as across 1 s during each trial of the five shoulder normalisation tests. The mean EMG levels across the trials were calculated for each test. Differences in the levels were examined using a 2 factor repeated measures analysis of variance (ANOVA) with factors: test and electrode type (Statistica, version 7.0, Stat Soft Inc., Tulsa, OK). The mean activation level from the lower fibres of serratus anterior as measured by the mean linear envelope of the EMG recorded using each type of electrode across each of the concentric and eccentric phases of movement, identified using the draw wire sensor signal, were calculated for each trial of each dynamic test
Fig. 2. An example of the ramped target signal (smooth line) and matched force applied by the subject (irregular line) as displayed on the computer screen during the isometric exercises.
and averaged across trials. Differences in the levels were examined using a 3 factor repeated measures ANOVA with factors: test, phase of movement and electrode type. Normality of the data was confirmed using probability plots. Tukey HSD post hoc analysis was used when significant ANOVA results were obtained. The signals were then time normalised to 101 points for each testing cycle and Pearson’s correlation analysis was used to assess the similarity in the pattern of change with load or range of movement between signals obtained from the two types of electrodes.
3. Results Mean (±95% CI) lower serratus activity levels recorded from both surface and intramuscular electrodes for each of the test conditions examined are depicted in Fig. 3. During the different ramped isometric tests, there was a significant difference between activity recorded from different tests (F3,18 = 31.01, p < 0.05) and an interaction between test and electrode type (F3,18 = 5.70, p < 0.05). Tukey post hoc analysis indicated that the activity recorded using the intramuscular electrodes was higher (p < 0.05) than that recorded using the surface electrodes during the ramped isometric shoulder abduction and flexion tests with no difference (p > 0.05) between the two electrode types during adduction and extension tests. Serratus anterior mean activity levels from each electrode type during abduction were similar (p = 1.0) to the levels recorded during flexion and both were higher than that recorded during shoulder adduction and extension (p < 0.05). During the dynamic tests, there was a main effect of: electrode type (F1,6 = 6.59, p < 0.05) with the intramuscular electrodes registering higher activity levels than surface electrodes; phase of movement (F1,6 = 54.59, p < 0.01) with higher levels of activity recorded during the concentric phase of each test; and with different tests producing different activity levels (F4,24 = 57.16, p < 0.01). There was also a three way interaction between test, electrode type and phase of movement (F4,24 = 4.97, p < 0.01). Tukey post hoc test indicated that the activity recorded using the intramuscular electrodes was higher (p < 0.05) than that recorded using the surface electrodes during the concentric phase of both dynamic abduction and flexion and during both the concentric and eccentric phases of the bench press plus with no differences between the two types of electrodes during any other tests or phases of movement (p > 0.05). Lower serratus anterior mean activity levels recorded with each electrode type during dynamic shoulder abduction, flexion and bench press were similar and higher than that recorded during dynamic adduction and extension (p < 0.05). During the isometric shoulder normalisation tests, there were significant main effects in: electrode type (F1,6 = 9.59, p < 0.05) with the intramuscular electrodes recording higher activity levels than the surface electrodes; differences between tests (F4,24 = 77.69, p < 0.01); and an interaction between test and electrode type (F4,24 = 5.61, p < 0.05). Tukey post hoc analysis indicated that activity in the lower fibres of serratus anterior recorded using the intramuscular electrodes was higher (p < 0.05) than that recorded using the surface electrodes during shoulder abduction at 90° in internal rotation and horizontal adduction with no difference (p > 0.05) between the two electrode types during flexion at 125°, extension at 30° abduction and internal rotation. The mean activity levels from each electrode type during abduction at 90° in internal rotation were similar (p > 0.05) to the levels during horizontal adduction and both were higher (p < 0.05) than during shoulder internal rotation and extension normalisation tests. Lower serratus anterior activity levels during flexion were similar (p = 0.64) to those recorded during abduction and higher than during all other normalisation tests (p < 0.05) when recorded by the
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L. Hackett et al. / Journal of Electromyography and Kinesiology 24 (2014) 221–227
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Fig. 3. Mean normalised serratus anterior activity levels (±95% CI) recorded from surface (grey) and intramuscular electrodes (black) electrodes during the tests investigated. * indicates significantly different mean activation levels between electrode types (p < 0.05).
serratus anterior activation level (% MVC)
intramuscular electrodes. Lower serratus anterior activity levels recorded by the surface electrodes were higher during flexion (p < 0.05) than all other normalisation tests. All other normalisation tests produced activity at an average of <10%MVC and no significant differences were found in serratus anterior activity levels recorded using intramuscular and surface electrodes (p > 0.05). The mean (±95% CI) time normalised activity levels in the lower fibres of serratus anterior as recorded from each electrode type for each of the ramped isometric and dynamic test conditions examined that produced mean activity levels >10% are depicted in Fig. 4. The mean (±95% CI) Pearson’s correlation coefficients across
subjects between lower serratus anterior activity recorded with intramuscular and surface electrodes during both the isometric ramped and dynamic tests were low (r 6 0.41) for the concentric phases of the dynamic abduction and flexion but high (r P 0.68) otherwise.
4. Discussion The results of this study provide no evidence to indicate that crosstalk is contaminating the signals recorded from the surface
a
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time (% cycle) Fig. 4. Mean time normalised pattern of normalised serratus anterior activation as recorded from intramuscular (black) and surface (grey) electrodes with 95% CI (dashed lines) versus time (% cycle) for (a) isometric ramp abduction, (b) isometric ramp flexion, (c) dynamic abduction, (d) dynamic flexion, and (e) bench press. The average (±95% confidence intervals) across subjects and trials of the correlation coefficient between the recordings from intramuscular and surface electrodes is reported.
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electrodes over the lower fibres of serratus anterior. During all the adduction and extension tasks examined, similarly low serratus anterior activity was recorded from both the intramuscular and surface electrodes (Johnson et al., 2011; Waite et al., 2010). This indicates that the surface electrodes were not picking up activity from adjacent muscles. However, this study has demonstrated significantly different activity in the lower fibres of serratus anterior recorded using surface electrodes and intramuscular electrodes during both dynamic and isometric shoulder tasks when serratus anterior would be expected to be active (Fig. 3). During shoulder flexion, abduction, bench press and horizontal adduction across all loads examined significantly lower serratus anterior activity levels were recorded from the surface electrodes compared with the intramuscular electrodes. This consistent under-reporting of serratus anterior activity by surface electromyography indicates that activity in the lower fibres of serratus anterior can only be measured validly with the use of intramuscular electromyography. A likely explanation of the significantly lower serratus anterior activity levels recorded using surface electromyography is geometric displacement. As the shoulder moved through range, the skin over the lower fibres of serratus anterior may have moved to a different position in relation to the muscle. This may have resulted in the surface electrodes being displaced to a position with greater fatty tissue and/or away from the innervation zone of the muscle, or off serratus anterior completely and into the intercostal space. The low correlation (Fig. 4) between the recruitment patterns of the lower fibres of serratus anterior recorded during the concentric phases of the dynamic shoulder flexion and abduction tasks examined would also indicate that the two recording electrode types detected significantly different patterns of activation and would support these explanations. Geometric displacement could also explain the significantly lower activity in the lower fibres of serratus anterior recorded by the surface electrodes during the shoulder isometric tasks performed at 90° elevation (flexion, abduction and horizontal flexion). The surface electrodes were attached with the subject’s arm abducted to 60°. Moving the arm to 90° flexion or abduction may have again displaced the surface electrodes away from the rib to which serratus anterior is attached and over the superior intercostal space. This was consistent with dynamic exercises where the greatest difference between the electrode types occurred at approximately 90° elevation (middle of the concentric range at 25% cycle, Fig. 4). However, during the isometric normalisation test performed at 125° flexion, there was no difference in the activity recorded from surface and intramuscular electrodes. During this test the surface electrodes may have displaced further superiorly from the intercostal space to be positioned over the rib above and therefore, over the digitation of serratus anterior attaching to this rib, and hence recorded similar activity to the intramuscular electrode. Based upon these findings, surface electrodes may validly record activity from the lower fibres of serratus anterior during isometric tasks if the surface electrodes are applied with the shoulder joint in the same angle at which isometric testing will be performed, therefore minimising potential electrode movement. The current study only compared serratus anterior muscle activity recorded using surface and intramuscular electrodes from the muscle attachment over rib 7. However, because the only superficial parts of serratus anterior accessible for surface electrode placements are over the slips attaching to the ribs, it is likely that geometric displacement would also affect the validity of surface electrode recordings from other rib locations. This will require further study to determine the applicability of the current results to parts of serratus anterior attaching to other ribs. The similar activation levels recorded between electrode types during the flexion shoulder normalisation test, where maximum
activity from the lower fibres of serratus anterior was most commonly recorded, suggests that intramuscular electromyography is at least as representative of muscle activity in lower serratus anterior as surface electromyography. With intramuscular electrodes recording greater lower serratus anterior activity than surface electrodes during abduction, flexion and bench press tests and similar levels in all other test conditions, it could be argued that they are in fact more representative than surface electrodes. This finding is consistent with other studies suggesting that intramuscular electromyography is representative of whole muscle activity in the shoulder region (Bogey et al., 2000; Bouisset and Maton, 1972; Johnson et al., 2011). While the results of the current study indicate that intramuscular electrodes are at least as representative of lower serratus anterior activity as surface electrodes, it is possible that neither electrode type was detecting activity from the entire muscle. In this experiment electrodes were placed over/into the part of serratus anterior associated with the 7th rib i.e. over the lower portion of serratus anterior. Future research will need to investigate both upper and lower sections of serratus anterior to determine if recording from only lower portions validly represents activity in the whole of this muscle. In conclusion, this study demonstrates that it is not valid to use surface electrodes placed over the digitation of serratus anterior attached to rib 7 to record muscle activity from the lower fibres of serratus anterior during dynamic exercises where serratus anterior would be expected to be active and isometric exercises where the electrodes are not placed at the shoulder angle to be tested. Additionally, intramuscular electrodes have been shown to be at least as representative of activity in the lower fibres of serratus anterior as surface electrodes. These results indicate that intramuscular electrodes should be used to investigate lower serratus anterior activation patterns during functional activities. Funding No funding was obtained for this study. Conflict of interest None declared. Photography All subjects photographed provided their consent by ticking applicable box in consent form. References Basmajian JV, De Luca CJ. Muscles alive, their functions revealed by electromyography. Baltimore: Williams & Wilkins; 1985. Boettcher CE, Ginn KA, Cathers I. Standard maximum isometric voluntary contraction tests for normalizing shoulder muscle EMG. J Orthop Res 2008;26(12):1591–7. Bogey RA, Perry J, Bontrager EL, Gronley JK. Comparison of across-subject EMG profiles using surface and multiple indwelling wire electrodes during gait. J Electromyogr Kinesiol 2000;10(4):255–9. Bouisset S, Maton B. Quantitative relationship between surface EMG and intramuscular electromyographic activity in voluntary movement. Am J Phys Med 1972;51(6):285. Brzycki M. Strength training – a practical approach to strength training, 3rd ed., Lincolnwood, Il: Masters Press; 1995. p. 86. Cools AM, Dewitte V, Lanszweert F, Notebaert D, Roets A, Soetens B, et al. Rehabilitation of scapular muscle balance: which exercises to prescribe? Am J Sports Med 2007;35(10):1744–51. Decker MJ, Hintermeister RA, Faber KJ, Hawkins RJ. Serratus anterior muscle activity during selected rehabilitation exercises. Am J Sports Med 1999;27(6):784–91. Ekstrom RA, Donatelli RA, Soderberg GL. Surface electromyographic analysis of exercises for the trapezius and serratus anterior muscles. J Orthop Sports Phys Ther 2003;33(5):247–58.
L. Hackett et al. / Journal of Electromyography and Kinesiology 24 (2014) 221–227 Ekstrom RA, Bifulco KM, Lopau CJ, Andersen CF, Gough JR. Comparing the function of the upper and lower parts of the serratus anterior muscle using surface electromyography. J. Orthop Sports Phys Ther 2004;34(5):235–43. Ekstrom RA, Soderberg GL, Donatelli RA. Normalization procedures using maximum voluntary isometric contractions for the serratus anterior and trapezius muscles during surface EMG analysis. J Electromyogr Kinesiol 2005;15(4):418–28. Geiringer S. Anatomic localization for needle electromyography: Steve R. Geiringer, MD Mosby, St. Louis, MO, 1994, 153 pp, US$28.95 ISBN 1-56053-068-5. J Electromyogr Kinesiol 1994;4(1):61. Ginn KA, Halaki M, Cathers I. Revision of the shoulder normalization tests is required to include rhomboid major and teres major. J Orthop Res 2011;29(12):1846–9. Giroux B, Lamontagne M. Comparison between surface and intramuscular wire electrodes in isometric and dynamic conditions. Electromyogr Clin Neurophysiol 1989;30:397–405. Hardwick DH, Beebe JA, McDonnell MK, Lang CE. A comparison of serratus anterior muscle activation during a wall slide exercise and other traditional exercises. J Orthop Sports Phys Ther 2006;36(12):903–10. Jaggi A, Malone AA, Cowan J, Lambert S, Bayley I, Cairns MC. Prospective blinded comparison of surface versus wire electromyographic analysis of muscle recruitment in shoulder instability. Physiother Res Int: J Researchers Clin Phys Ther 2009;14(1):17–29. Johnson VL, Halaki M, Ginn KA. The use of surface electrodes to record infraspinatus activity is not valid at low infraspinatus activation levels. J Electromyo Kines: Off J Int Soc Electrophysiol Kines 2011;21(1):112–8. Ludewig PM, Hoff MS, Osowski EE, Meschke SA, Rundquist PJ. Relative balance of serratus anterior and upper trapezius muscle activity during push-up exercises. Am J Sports Med 2004;32(2):484–93. Oberg T, SandsJo L, Kadefors R. Arm movement and EMG mean power frequency in the trapezius muscle: a comparison between surface and intramuscular recording techniques. Electromyogr Clin Neurophysiol 1992;32(1–2):87–96. Palastanga N, Field D, Soames R. Anatomy and human movement – structure and function. Edinburgh: Butterworth-Heinemann Elsevier; 2012. Perry J, Easterday CS, Antonelli DJ. Surface versus intramuscular electrodes for electromyography of superficial and deep muscles. Phys Ther 1981;61(1):7. Stokes IAF, Henry SM, Single RM. Surface EMG electrodes do not accurately record from lumbar multifidus muscles. Clin Biomech 2003;18(1):9–13. Waite DL, Brookham RL, Dickerson CR. On the suitability of using surface electrode placements to estimate muscle activity of the rotator cuff as recorded by intramuscular electrodes. J Electromyo Kines: Off J Int Soc Electrophysiol Kines 2010;20(5):903–11. Yemm R. The representation of motor-unit action-potentials on skin-surface electromyograms of the masseter and temporal muscles in man. Arch Oral Biol 1977;22(3):201–5.
Lucien Hackett is a medical student at the University of Sydney. He graduated with first class honours in Exercise and Sport Science from the Faculty of Health Sciences, University of Sydney in 2012. He has specific interests in the areas of anatomy and sports medicine.
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Darren Reed is a lecturer in the Discipline of Biomedical Science, Sydney Medical School, The University of Sydney and a musculoskeletal physiotherapist in part time private practice. He is currently enrolled in a Doctorate in Philosophy using electromyography to investigate shoulder muscle activation patterns in normal subjects during rehabilitation exercises and functional movements.
Mark Halaki is currently a senior lecturer in the Discipline of Exercise and Sport Science, The Faculty of Health Sciences, The University of Sydney. He has a background in mechanical and biomedical engineering with research interests in electromyographic studies in the areas of motor control and biomechanics.
Karen Ginn is a musculoskeletal anatomist in the Discipline of Biomedical Science, Sydney Medical School, The University of Sydney and a musculoskeletal physiotherapist in part time private practice. She is involved in research related to the examination and treatment of shoulder dysfunction including: electromyographic studies investigating shoulder muscle activity patterns in normal subjects and patients with shoulder dysfucntion; clinical trials investigating the effectiveness of treatment for shoulder dysfunction; the aetiology of frozen shoulder; perceptual changes associated with chronic shoulder pain; and studies evaluating the validity of physical examination techniques at the shoulder.
Contents lists available at ScienceDirect
Journal of Electromyography and Kinesiology journal homepage: www.elsevier.com/locate/jelekin
Assessing the validity of surface electromyography for recording muscle activation patterns from serratus anterior Lucien Hackett a, Darren Reed b,⇑, Mark Halaki a, Karen A. Ginn b a b
Discipline of Exercise and Sport Science, Faculty of Health Sciences, The University of Sydney, Australia Discipline of Biomedical Science, Sydney Medical School, The University of Sydney, Australia
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Article history: Received 27 June 2013 Received in revised form 10 January 2014 Accepted 17 January 2014
Keywords: Shoulder Serratus anterior Muscle activation Electromyography
a b s t r a c t Purpose: No direct evidence exists to support the validity of using surface electrodes to record muscle activity from serratus anterior, an important and commonly investigated shoulder muscle. The aims of this study were to determine the validity of examining muscle activation patterns in serratus anterior using surface electromyography and to determine whether intramuscular electromyography is representative of serratus anterior muscle activity. Methods: Seven asymptomatic subjects performed dynamic and isometric shoulder flexion, extension, abduction, adduction and dynamic bench press plus tests. Surface electrodes were placed over serratus anterior and around intramuscular electrodes in serratus anterior. Load was ramped during isometric tests from 0% to 100% maximum load and dynamic tests were performed at 70% maximum load. EMG signals were normalised using five standard maximum voluntary contraction tests. Results: Surface electrodes significantly underestimated serratus anterior muscle activity compared with the intramuscular electrodes during dynamic flexion, dynamic abduction, isometric flexion, isometric abduction and bench press plus tests. All other test conditions showed no significant differences including the flexion normalisation test where maximum activation was recorded from both electrode types. Low correlation between signals was recorded using surface and intramuscular electrodes during concentric phases of dynamic abduction and flexion. Conclusions: It is not valid to use surface electromyography to assess muscle activation levels in serratus anterior during isometric exercises where the electrodes are not placed at the angle of testing and dynamic exercises. Intramuscular electrodes are as representative of the serratus anterior muscle activity as surface electrodes. Ó 2014 Elsevier Ltd. All rights reserved.
1. Introduction Electromyography (EMG) is the most reliable tool that researchers have to understand the complex activation patterns of muscles during exercises and functional activities (Basmajian and De Luca, 1985). EMG can be recorded by intramuscular electrodes placed into the belly of the muscle or surface electrodes placed on the overlying skin. Traditionally surface electrodes have been preferred for superficial muscles as they are non-invasive, easier to set up (Giroux and Lamontagne, 1989) and sample from a larger cross-section of the muscle than intramuscular electrodes (Basmajian and De Luca, 1985). However, surface electrodes may be susceptible to geometric ⇑ Corresponding author. Address: Discipline of Biomedical Science, Sydney Medical School, Cumberland Campus C42, The University of Sydney, Lidcombe, NSW 1825, Australia. Tel.: +61 2 9351 9144; fax: +61 2 9351 9715. E-mail address: [email protected] (D. Reed). http://dx.doi.org/10.1016/j.jelekin.2014.01.007 1050-6411/Ó 2014 Elsevier Ltd. All rights reserved.
displacement away from the target muscle (Oberg et al., 1992) and recording EMG signals from adjacent or underlying muscles, leading to contamination of signals, known as crosstalk (Johnson et al., 2011; Perry et al., 1981; Stokes et al., 2003). Intramuscular electrodes are commonly used to record activity from deep muscles inaccessible to surface electrodes, but may also be the electrode of choice in some superficial muscles if cross talk or geometric displacement is a potential problem. They record activity from a smaller volume of muscle having more specificity than surface electrodes and therefore, are not susceptible to crosstalk (Basmajian and De Luca, 1985; Bouisset and Maton, 1972; Giroux and Lamontagne, 1989). However, studies suggest that they may not be representative of activity in the entire muscle (Giroux and Lamontagne, 1989; Yemm, 1977). The shoulder region, with the humerus and scapula both moving through large ranges and multiple muscles with varying morphology lying in close proximity to each other, presents challenges in using surface electrodes on superficial shoulder muscles.
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Previous research in the shoulder region has shown geometric displacement (Oberg et al., 1992) and crosstalk from adjacent muscles in isometric (Johnson et al., 2011; Waite et al., 2010) and dynamic exercises (Jaggi et al., 2009) may lead to invalid recordings from surface electrodes. Serratus anterior is an important axioscapular muscle crucial to normal shoulder function. This large, flat muscular sheet attaches via individual digitations from the first 8 or 9 ribs to the medial border of the scapula (Palastanga et al., 2012). It is a major protractor of the scapula and the lower fibres co-ordinate with trapezius to upwardly rotate the scapula (Palastanga et al., 2012). EMG research investigating serratus anterior activity has predominantly used surface electromyography over the lower digitations of the muscle where it is most accessible and superficial (Cools et al., 2007; Decker et al., 1999; Ekstrom et al., 2003). However, glenohumeral joint movement results in the skin overlying the lower fibres of serratus anterior experiencing large degrees of shift during shoulder movement. There is also the possibility that surface electrode recordings from serratus anterior may be contaminated by potential cross-talk from adjacent muscles. To date, no studies have assessed the validity of using surface electrodes to record activity from serratus anterior. In addition, the issue of whether recording serratus anterior activity using intramuscular electrodes is representative of activity in the whole of this large muscle has not been investigated and is still unknown. Therefore, the aims of this experiment were to: Determine the validity of using surface electrodes to record muscle activity from the lower fibres of serratus anterior during dynamic and isometric contractions. In the test conditions where the validity of surface electrode recordings were confirmed, to determine the representativeness of intramuscular electrodes compared to surface electrodes for recording muscle activity from the lower fibres of serratus anterior. 2. Methods 2.1. Subjects Seven asymptomatic subjects (six male, one female, aged 19– 23) volunteered to participate in this investigation. To be eligible to participate subjects must have had no pain in their dominant shoulder in the previous two years and had never been treated for shoulder pain. Prior to the experiment, shoulder strength and range of motion tests were conducted by an experienced physiotherapist to verify normal pain free functioning of the dominant shoulder and subjects gave their informed consent. Ethics approval was granted by The University of Sydney’s Human Research Ethics Committee (approval number 04-2011/13610). 2.2. Instrumentation Electromyographic data were collected simultaneously from the lower fibres of serratus anterior using both surface and intramuscular electrodes. Intramuscular electrodes were manufactured in the Shoulder Laboratory, Sydney Medical School, using the technique developed by Basmajian and De Luca (1985) and comprised of two insulated wires of 0.14 mm diameter made of Teflon coated stainless steel. The two wires were bent back to form barbs at 2 mm and 4 mm respectively from the terminal end. This terminal end was de-insulated for a length of 1 mm for both wires. Using a sterile technique, the wires were inserted via a hypodermic needle acting as a cannula into the digitation of serratus anterior over rib 7 (Geiringer, 1994). Wires were looped to allow for adequate movement, and then taped to the skin to prevent inadvertent removal.
A pair of 3.2 mm diameter silver/sliver chloride surface electrodes (Red Dot, 2258, 3M, Sydney, Australia) was used to detect muscle activity from serratus anterior (Ekstrom et al., 2004). With the subject side-lying and the arm in 60° abduction, the surface electrodes for serratus anterior were placed at a distance of approximately 25 mm apart over the seventh rib (Ekstrom et al., 2005; Hardwick et al., 2006), in line with the muscle fibres and around the intramuscular electrodes (Giroux and Lamontagne, 1989; Johnson et al., 2011). A large ground electrode (Universal Electrosurgical Pad: Split, 9160F, 3M, Sydney, Australia) was placed on the spine and acromion of the contralateral scapula. Resistances were measured between surface electrodes (Dick Smith Electronics Q-1450) and were <5 kX. Both the intramuscular and surface electrodes were then connected to amplifiers (Iso-DAM8-8 amplifiers, World Precision Instruments, Sarasota, FL; gain = 100) via a junction box. Data was recorded on a personal computer using SPIKE 2 software (Version 4.0 Cambridge Electronics Design, Cambridge, UK) and a 16 channel analogue to digital converter (CED2701, CED Ltd., Cambridge, UK) at a sample rate of 3125 Hz. Maximum voluntary contractions (MVCs) were then performed using five standardised shoulder normalisation tests (Boettcher et al., 2008; Ginn et al., 2011) known to have a high likelihood of producing maximum activity in serratus anterior. These normalisation tests were performed in random order and consisted of manually resisted shoulder flexion with the shoulder at 125° flexion, internal rotation at 90° shoulder abduction, shoulder extension at 30° abduction, abduction with the shoulder abducted 90° and internally rotated and self-resisted horizontal adduction at 90° shoulder flexion. 2.3. Test positions Isometric and dynamic tests of shoulder flexion, extension, abduction, adduction and a dynamic bench press plus exercise (seated chest press to a point where the elbows are fully extended, followed by shoulder protraction) were performed. These tests were selected as they include tasks expected to elicit high serratus anterior activity (flexion and abduction, bench press plus) (Decker et al., 1999; Ludewig et al., 2004), as well as ones in which it would be expected to be less active (extension, adduction). The order of the isometric and dynamic tests was block randomised. During the abduction, adduction, flexion and extension tests the subject stood with their feet placed shoulder width apart and their contralateral hand placed on the corresponding hip in order to prevent unwanted trunk movement. For the flexion test, the contralateral foot was brought two feet-lengths forward, and for the extension test, the ipsilateral foot was brought two feet-lengths forward. The bench press plus exercise was performed on gym equipment (Hyper Extension Gym 50036, 150lbs). Prior to testing and electrode placement, the maximum isometric load (100% load) for shoulder abduction, flexion, adduction, and extension was measured using a load cell (XTRAN load cell S1W, Applied Measurement Australia PTY LTD, Melbourne, Australia), with resistance maintained for three seconds. Maximum tests were repeated twice, with at least a 30 s rest in between each repetition. The maximum load was used as the ramped isometric target load, and to calculate the 70% maximum load used during dynamic testing. The one repetition maximum (1RM) for the dynamic bench press plus exercise was calculated by the Bryzcki equation, using the number of repetitions a subject was able to perform sub-maximally to determine their 1RM (Bryzcki, 1995). The testing order of these maximal load tests was randomised. Dynamic tests included shoulder flexion, extension, abduction, adduction and bench press plus. The bench press plus, was performed seated and through range from 20° shoulder extension to 90° shoulder flexion, followed by full range scapular protraction
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F
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E i) Fig. 1. Performance of flexion (A), extension (B), abduction (C), adduction (D), bench press plus (E) during both dynamic (i) and isometric (ii) conditions. Force transducer (F).
(Fig. 1E). The other four shoulder movements were performed using a cable apparatus attached to a pulley (Fig. 1A–D). Abduction was performed from 0° to 160°, adduction from 140° to 0°, flexion from 30° extension to 160° flexion and extension from 140° flexion to 30° extension. Load was set at 70% of maximum load during these dynamic tests in order to produce a high level of muscle activity while avoiding the level of fatigue that comes with prolonged maximal exercise. Timing was monitored and standardised at three seconds during the concentric phase and three seconds during the eccentric phase of the exercises, with a one second pause between concentric and eccentric phases. The same body and foot positioning as
described above was monitored in order to ensure correct scapulohumeral rhythm during the execution of each test without compensatory trunk movement. A draw-wire was used (Microepsilon, 94496, Ortenburg, Germany) to synchronise shoulder movement with the EMG signals. Two repetitions of each dynamic test were performed in random order, with a 30 s rest interval between each repetition. Ramped isometric tests for shoulder flexion, extension, abduction, and adduction were performed randomly with at least 2 min rest between each test to avoid the effects of fatigue. Ramped exercises allowed for an examination of the effect of different isometric loads ranging from 0% to 100% of maximum
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load. Posture and feet positioning was monitored and standardised as in the dynamic tests. Using the load cell (XTRAN load cell S1W, Applied Measurement Australia PTY LTD, Melbourne, Australia) connected to an amplifier (DA100 BIOPAC Systems Inc, Goleta, CA USA) connected to an analogue to digital converter (MP100, BIOPAC Systems Inc, Goleta, CA, USA) and the AcqKnowledge Software (Version 3.9.0, BIOPAC Systems Inc, Goleta, CA, USA), subjects’ applied force and target force signals were displayed on a laptop computer. The ramped target signal consisted of a four seconds linear increase in force from zero to maximum, three seconds at maximum, then four seconds linear decrease back to zero (Fig. 2). Subjects were instructed to follow the target signal by applying the appropriate force level. Isometric tests were performed in standing using the same pulley apparatus as for the majority of the dynamic shoulder tests. The shoulder was positioned in 90° flexion in the sagittal plane for the flexion and extension tests and in 90° abduction in the scapular plane for the abduction and adduction tests. The isometric tests were performed twice in random order, with a 30 s rest interval between repetitions.
2.4. Data analysis Data processing was performed in Matlab (version 7, The Math Works, Natick, MA). EMG signals were high pass filtered at 10 Hz (zero lag, 8th Order Butterworth), notch filtered at 50 Hz (zero lag, 8th Order Butterworth), rectified then the linear envelope calculated by low pass filtering at 3 Hz (zero lag, 8th Order Butterworth). The EMG signals were then normalised using the maximum value recorded for the muscle during the five normalisation tests and expressed as (%MVC) separately for each of the surface and indwelling electrodes. The mean activation level from the lower fibres of serratus anterior as measured by the mean linear envelope of the EMG recorded using each type of electrode across each trial of each isometric test was calculated as well as across 1 s during each trial of the five shoulder normalisation tests. The mean EMG levels across the trials were calculated for each test. Differences in the levels were examined using a 2 factor repeated measures analysis of variance (ANOVA) with factors: test and electrode type (Statistica, version 7.0, Stat Soft Inc., Tulsa, OK). The mean activation level from the lower fibres of serratus anterior as measured by the mean linear envelope of the EMG recorded using each type of electrode across each of the concentric and eccentric phases of movement, identified using the draw wire sensor signal, were calculated for each trial of each dynamic test
Fig. 2. An example of the ramped target signal (smooth line) and matched force applied by the subject (irregular line) as displayed on the computer screen during the isometric exercises.
and averaged across trials. Differences in the levels were examined using a 3 factor repeated measures ANOVA with factors: test, phase of movement and electrode type. Normality of the data was confirmed using probability plots. Tukey HSD post hoc analysis was used when significant ANOVA results were obtained. The signals were then time normalised to 101 points for each testing cycle and Pearson’s correlation analysis was used to assess the similarity in the pattern of change with load or range of movement between signals obtained from the two types of electrodes.
3. Results Mean (±95% CI) lower serratus activity levels recorded from both surface and intramuscular electrodes for each of the test conditions examined are depicted in Fig. 3. During the different ramped isometric tests, there was a significant difference between activity recorded from different tests (F3,18 = 31.01, p < 0.05) and an interaction between test and electrode type (F3,18 = 5.70, p < 0.05). Tukey post hoc analysis indicated that the activity recorded using the intramuscular electrodes was higher (p < 0.05) than that recorded using the surface electrodes during the ramped isometric shoulder abduction and flexion tests with no difference (p > 0.05) between the two electrode types during adduction and extension tests. Serratus anterior mean activity levels from each electrode type during abduction were similar (p = 1.0) to the levels recorded during flexion and both were higher than that recorded during shoulder adduction and extension (p < 0.05). During the dynamic tests, there was a main effect of: electrode type (F1,6 = 6.59, p < 0.05) with the intramuscular electrodes registering higher activity levels than surface electrodes; phase of movement (F1,6 = 54.59, p < 0.01) with higher levels of activity recorded during the concentric phase of each test; and with different tests producing different activity levels (F4,24 = 57.16, p < 0.01). There was also a three way interaction between test, electrode type and phase of movement (F4,24 = 4.97, p < 0.01). Tukey post hoc test indicated that the activity recorded using the intramuscular electrodes was higher (p < 0.05) than that recorded using the surface electrodes during the concentric phase of both dynamic abduction and flexion and during both the concentric and eccentric phases of the bench press plus with no differences between the two types of electrodes during any other tests or phases of movement (p > 0.05). Lower serratus anterior mean activity levels recorded with each electrode type during dynamic shoulder abduction, flexion and bench press were similar and higher than that recorded during dynamic adduction and extension (p < 0.05). During the isometric shoulder normalisation tests, there were significant main effects in: electrode type (F1,6 = 9.59, p < 0.05) with the intramuscular electrodes recording higher activity levels than the surface electrodes; differences between tests (F4,24 = 77.69, p < 0.01); and an interaction between test and electrode type (F4,24 = 5.61, p < 0.05). Tukey post hoc analysis indicated that activity in the lower fibres of serratus anterior recorded using the intramuscular electrodes was higher (p < 0.05) than that recorded using the surface electrodes during shoulder abduction at 90° in internal rotation and horizontal adduction with no difference (p > 0.05) between the two electrode types during flexion at 125°, extension at 30° abduction and internal rotation. The mean activity levels from each electrode type during abduction at 90° in internal rotation were similar (p > 0.05) to the levels during horizontal adduction and both were higher (p < 0.05) than during shoulder internal rotation and extension normalisation tests. Lower serratus anterior activity levels during flexion were similar (p = 0.64) to those recorded during abduction and higher than during all other normalisation tests (p < 0.05) when recorded by the
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Fig. 3. Mean normalised serratus anterior activity levels (±95% CI) recorded from surface (grey) and intramuscular electrodes (black) electrodes during the tests investigated. * indicates significantly different mean activation levels between electrode types (p < 0.05).
serratus anterior activation level (% MVC)
intramuscular electrodes. Lower serratus anterior activity levels recorded by the surface electrodes were higher during flexion (p < 0.05) than all other normalisation tests. All other normalisation tests produced activity at an average of <10%MVC and no significant differences were found in serratus anterior activity levels recorded using intramuscular and surface electrodes (p > 0.05). The mean (±95% CI) time normalised activity levels in the lower fibres of serratus anterior as recorded from each electrode type for each of the ramped isometric and dynamic test conditions examined that produced mean activity levels >10% are depicted in Fig. 4. The mean (±95% CI) Pearson’s correlation coefficients across
subjects between lower serratus anterior activity recorded with intramuscular and surface electrodes during both the isometric ramped and dynamic tests were low (r 6 0.41) for the concentric phases of the dynamic abduction and flexion but high (r P 0.68) otherwise.
4. Discussion The results of this study provide no evidence to indicate that crosstalk is contaminating the signals recorded from the surface
a
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time (% cycle) Fig. 4. Mean time normalised pattern of normalised serratus anterior activation as recorded from intramuscular (black) and surface (grey) electrodes with 95% CI (dashed lines) versus time (% cycle) for (a) isometric ramp abduction, (b) isometric ramp flexion, (c) dynamic abduction, (d) dynamic flexion, and (e) bench press. The average (±95% confidence intervals) across subjects and trials of the correlation coefficient between the recordings from intramuscular and surface electrodes is reported.
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electrodes over the lower fibres of serratus anterior. During all the adduction and extension tasks examined, similarly low serratus anterior activity was recorded from both the intramuscular and surface electrodes (Johnson et al., 2011; Waite et al., 2010). This indicates that the surface electrodes were not picking up activity from adjacent muscles. However, this study has demonstrated significantly different activity in the lower fibres of serratus anterior recorded using surface electrodes and intramuscular electrodes during both dynamic and isometric shoulder tasks when serratus anterior would be expected to be active (Fig. 3). During shoulder flexion, abduction, bench press and horizontal adduction across all loads examined significantly lower serratus anterior activity levels were recorded from the surface electrodes compared with the intramuscular electrodes. This consistent under-reporting of serratus anterior activity by surface electromyography indicates that activity in the lower fibres of serratus anterior can only be measured validly with the use of intramuscular electromyography. A likely explanation of the significantly lower serratus anterior activity levels recorded using surface electromyography is geometric displacement. As the shoulder moved through range, the skin over the lower fibres of serratus anterior may have moved to a different position in relation to the muscle. This may have resulted in the surface electrodes being displaced to a position with greater fatty tissue and/or away from the innervation zone of the muscle, or off serratus anterior completely and into the intercostal space. The low correlation (Fig. 4) between the recruitment patterns of the lower fibres of serratus anterior recorded during the concentric phases of the dynamic shoulder flexion and abduction tasks examined would also indicate that the two recording electrode types detected significantly different patterns of activation and would support these explanations. Geometric displacement could also explain the significantly lower activity in the lower fibres of serratus anterior recorded by the surface electrodes during the shoulder isometric tasks performed at 90° elevation (flexion, abduction and horizontal flexion). The surface electrodes were attached with the subject’s arm abducted to 60°. Moving the arm to 90° flexion or abduction may have again displaced the surface electrodes away from the rib to which serratus anterior is attached and over the superior intercostal space. This was consistent with dynamic exercises where the greatest difference between the electrode types occurred at approximately 90° elevation (middle of the concentric range at 25% cycle, Fig. 4). However, during the isometric normalisation test performed at 125° flexion, there was no difference in the activity recorded from surface and intramuscular electrodes. During this test the surface electrodes may have displaced further superiorly from the intercostal space to be positioned over the rib above and therefore, over the digitation of serratus anterior attaching to this rib, and hence recorded similar activity to the intramuscular electrode. Based upon these findings, surface electrodes may validly record activity from the lower fibres of serratus anterior during isometric tasks if the surface electrodes are applied with the shoulder joint in the same angle at which isometric testing will be performed, therefore minimising potential electrode movement. The current study only compared serratus anterior muscle activity recorded using surface and intramuscular electrodes from the muscle attachment over rib 7. However, because the only superficial parts of serratus anterior accessible for surface electrode placements are over the slips attaching to the ribs, it is likely that geometric displacement would also affect the validity of surface electrode recordings from other rib locations. This will require further study to determine the applicability of the current results to parts of serratus anterior attaching to other ribs. The similar activation levels recorded between electrode types during the flexion shoulder normalisation test, where maximum
activity from the lower fibres of serratus anterior was most commonly recorded, suggests that intramuscular electromyography is at least as representative of muscle activity in lower serratus anterior as surface electromyography. With intramuscular electrodes recording greater lower serratus anterior activity than surface electrodes during abduction, flexion and bench press tests and similar levels in all other test conditions, it could be argued that they are in fact more representative than surface electrodes. This finding is consistent with other studies suggesting that intramuscular electromyography is representative of whole muscle activity in the shoulder region (Bogey et al., 2000; Bouisset and Maton, 1972; Johnson et al., 2011). While the results of the current study indicate that intramuscular electrodes are at least as representative of lower serratus anterior activity as surface electrodes, it is possible that neither electrode type was detecting activity from the entire muscle. In this experiment electrodes were placed over/into the part of serratus anterior associated with the 7th rib i.e. over the lower portion of serratus anterior. Future research will need to investigate both upper and lower sections of serratus anterior to determine if recording from only lower portions validly represents activity in the whole of this muscle. In conclusion, this study demonstrates that it is not valid to use surface electrodes placed over the digitation of serratus anterior attached to rib 7 to record muscle activity from the lower fibres of serratus anterior during dynamic exercises where serratus anterior would be expected to be active and isometric exercises where the electrodes are not placed at the shoulder angle to be tested. Additionally, intramuscular electrodes have been shown to be at least as representative of activity in the lower fibres of serratus anterior as surface electrodes. These results indicate that intramuscular electrodes should be used to investigate lower serratus anterior activation patterns during functional activities. Funding No funding was obtained for this study. Conflict of interest None declared. Photography All subjects photographed provided their consent by ticking applicable box in consent form. References Basmajian JV, De Luca CJ. Muscles alive, their functions revealed by electromyography. Baltimore: Williams & Wilkins; 1985. Boettcher CE, Ginn KA, Cathers I. Standard maximum isometric voluntary contraction tests for normalizing shoulder muscle EMG. J Orthop Res 2008;26(12):1591–7. Bogey RA, Perry J, Bontrager EL, Gronley JK. Comparison of across-subject EMG profiles using surface and multiple indwelling wire electrodes during gait. J Electromyogr Kinesiol 2000;10(4):255–9. Bouisset S, Maton B. Quantitative relationship between surface EMG and intramuscular electromyographic activity in voluntary movement. Am J Phys Med 1972;51(6):285. Brzycki M. Strength training – a practical approach to strength training, 3rd ed., Lincolnwood, Il: Masters Press; 1995. p. 86. Cools AM, Dewitte V, Lanszweert F, Notebaert D, Roets A, Soetens B, et al. Rehabilitation of scapular muscle balance: which exercises to prescribe? Am J Sports Med 2007;35(10):1744–51. Decker MJ, Hintermeister RA, Faber KJ, Hawkins RJ. Serratus anterior muscle activity during selected rehabilitation exercises. Am J Sports Med 1999;27(6):784–91. Ekstrom RA, Donatelli RA, Soderberg GL. Surface electromyographic analysis of exercises for the trapezius and serratus anterior muscles. J Orthop Sports Phys Ther 2003;33(5):247–58.
L. Hackett et al. / Journal of Electromyography and Kinesiology 24 (2014) 221–227 Ekstrom RA, Bifulco KM, Lopau CJ, Andersen CF, Gough JR. Comparing the function of the upper and lower parts of the serratus anterior muscle using surface electromyography. J. Orthop Sports Phys Ther 2004;34(5):235–43. Ekstrom RA, Soderberg GL, Donatelli RA. Normalization procedures using maximum voluntary isometric contractions for the serratus anterior and trapezius muscles during surface EMG analysis. J Electromyogr Kinesiol 2005;15(4):418–28. Geiringer S. Anatomic localization for needle electromyography: Steve R. Geiringer, MD Mosby, St. Louis, MO, 1994, 153 pp, US$28.95 ISBN 1-56053-068-5. J Electromyogr Kinesiol 1994;4(1):61. Ginn KA, Halaki M, Cathers I. Revision of the shoulder normalization tests is required to include rhomboid major and teres major. J Orthop Res 2011;29(12):1846–9. Giroux B, Lamontagne M. Comparison between surface and intramuscular wire electrodes in isometric and dynamic conditions. Electromyogr Clin Neurophysiol 1989;30:397–405. Hardwick DH, Beebe JA, McDonnell MK, Lang CE. A comparison of serratus anterior muscle activation during a wall slide exercise and other traditional exercises. J Orthop Sports Phys Ther 2006;36(12):903–10. Jaggi A, Malone AA, Cowan J, Lambert S, Bayley I, Cairns MC. Prospective blinded comparison of surface versus wire electromyographic analysis of muscle recruitment in shoulder instability. Physiother Res Int: J Researchers Clin Phys Ther 2009;14(1):17–29. Johnson VL, Halaki M, Ginn KA. The use of surface electrodes to record infraspinatus activity is not valid at low infraspinatus activation levels. J Electromyo Kines: Off J Int Soc Electrophysiol Kines 2011;21(1):112–8. Ludewig PM, Hoff MS, Osowski EE, Meschke SA, Rundquist PJ. Relative balance of serratus anterior and upper trapezius muscle activity during push-up exercises. Am J Sports Med 2004;32(2):484–93. Oberg T, SandsJo L, Kadefors R. Arm movement and EMG mean power frequency in the trapezius muscle: a comparison between surface and intramuscular recording techniques. Electromyogr Clin Neurophysiol 1992;32(1–2):87–96. Palastanga N, Field D, Soames R. Anatomy and human movement – structure and function. Edinburgh: Butterworth-Heinemann Elsevier; 2012. Perry J, Easterday CS, Antonelli DJ. Surface versus intramuscular electrodes for electromyography of superficial and deep muscles. Phys Ther 1981;61(1):7. Stokes IAF, Henry SM, Single RM. Surface EMG electrodes do not accurately record from lumbar multifidus muscles. Clin Biomech 2003;18(1):9–13. Waite DL, Brookham RL, Dickerson CR. On the suitability of using surface electrode placements to estimate muscle activity of the rotator cuff as recorded by intramuscular electrodes. J Electromyo Kines: Off J Int Soc Electrophysiol Kines 2010;20(5):903–11. Yemm R. The representation of motor-unit action-potentials on skin-surface electromyograms of the masseter and temporal muscles in man. Arch Oral Biol 1977;22(3):201–5.
Lucien Hackett is a medical student at the University of Sydney. He graduated with first class honours in Exercise and Sport Science from the Faculty of Health Sciences, University of Sydney in 2012. He has specific interests in the areas of anatomy and sports medicine.
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Darren Reed is a lecturer in the Discipline of Biomedical Science, Sydney Medical School, The University of Sydney and a musculoskeletal physiotherapist in part time private practice. He is currently enrolled in a Doctorate in Philosophy using electromyography to investigate shoulder muscle activation patterns in normal subjects during rehabilitation exercises and functional movements.
Mark Halaki is currently a senior lecturer in the Discipline of Exercise and Sport Science, The Faculty of Health Sciences, The University of Sydney. He has a background in mechanical and biomedical engineering with research interests in electromyographic studies in the areas of motor control and biomechanics.
Karen Ginn is a musculoskeletal anatomist in the Discipline of Biomedical Science, Sydney Medical School, The University of Sydney and a musculoskeletal physiotherapist in part time private practice. She is involved in research related to the examination and treatment of shoulder dysfunction including: electromyographic studies investigating shoulder muscle activity patterns in normal subjects and patients with shoulder dysfucntion; clinical trials investigating the effectiveness of treatment for shoulder dysfunction; the aetiology of frozen shoulder; perceptual changes associated with chronic shoulder pain; and studies evaluating the validity of physical examination techniques at the shoulder.