Analysis and Biophysics of Surface EMG for Physiotherapists and Kinesiologists: Toward a Common Language With Rehabilitation Engineers
Lara McManus, Giuseppe De Vito, Madeleine M Lowery, Lara McManus, Giuseppe De Vito, Madeleine M Lowery
Abstract
Recent decades have seen a move toward evidence-based medicine to inform the clinical decision-making process with reproducible findings from high-quality research studies. There is a need for objective, quantitative measurement tools to increase the reliability and reproducibility of studies evaluating the efficacy of healthcare interventions, particularly in the field of physical and rehabilitative medicine. Surface electromyography (sEMG) is a non-invasive measure of muscle activity that is widely used in research but is under-utilized as a clinical tool in rehabilitative medicine. Other types of electrophysiological signals (e.g., electrocardiography, electroencephalography, intramuscular EMG) are commonly recorded by healthcare practitioners, however, sEMG has yet to successfully transition to clinical practice. Surface EMG has clear clinical potential as an indicator of muscle activation, however reliable extraction of information requires knowledge of the appropriate methods for recording and analyzing sEMG and an understanding of the underlying biophysics. These concepts are generally not covered in sufficient depth in the standard curriculum for physiotherapists and kinesiologists to encourage a confident use of sEMG in clinical practice. In addition, the common perception of sEMG as a specialized topic means that the clinical potential of sEMG and the pathways to application in practice are often not apparent. The aim of this paper is to address barriers to the translation of sEMG by emphasizing its benefits as an objective clinical tool and by overcoming its perceived complexity. The many useful clinical applications of sEMG are highlighted and examples provided to illustrate how it can be implemented in practice. The paper outlines how fundamental biophysics and EMG signal processing concepts could be presented to a non-technical audience. An accompanying tutorial with sample data and code is provided which could be used as a tool for teaching or self-guided learning. The importance of observing sEMG in routine use in clinic is identified as an essential part of the effective communication of sEMG recording and signal analysis methods. Highlighting the advantages of sEMG as a clinical tool and reducing its perceived complexity could bridge the gap between theoretical knowledge and practical application and provide the impetus for the widespread use of sEMG in clinic.
Keywords: clinical application; kinesiology; physiotherapy; rehabilitation; surface EMG tutorial; surface electromography.
Copyright © 2020 McManus, De Vito and Lowery.
Figures
References
- Rogers EM. Diffusion of Innovations, 4th ed New York, NY: Free Press; (1995).
- Jette AM. (2017). Overcoming ignorance and ineptitude in 21st century rehabilitation. Phys Ther. (2017) 97:497–98. 10.1093/ptj/pzx037
- Hunt A, Adamson B, Higgs J, Harris L. University education and the physiotherapy professional. Physiotherapy. (1998) 84:264–73. 10.1016/S0031-9406(05)65527-7
- Criswell E. Cram's Introduction to Surface Electromyography, 2nd ed Sudbury, MA: Jones & Bartlett Publishers; (2010).
- Kamen G, Gabriel DA. Essentials of Electromyography, 1st ed Champaign, IL: Human Kinetics; (2010).
- Barbero M, Merletti R, Rainoldi A. Atlas of Muscle Innervation Zones: Understanding Surface Electromyography and its Applications. Milan: Springer; (2012). 10.1007/978-88-470-2463-2
- Robertson GE, Caldwell GE, Hamill J, Kamen G, Whittlesey S. Research Methods in Biomechanics, 2nd ed Champaign, IL: Human kinetics; (2013). 10.5040/9781492595809
- Barry DT. AAEM minimonograph# 36: basic concepts of electricity and electronics in clinical electromyography. Muscle Nerve. (1991) 14:937–46. 10.1002/mus.880141003
- de Luca CJ. Physiology and mathematics of myoelectric signals. IEEE Trans Biomed Eng. (1979) 26:313–25. 10.1109/TBME.1979.326534
- Kamen G, Caldwell GE. Physiology and interpretation of the electromyogram. J Clin Neurophysiol. (1996) 13:366–84. 10.1097/00004691-199609000-00002
- Moritani T, Stegeman D, Merletti R. Basic physiology and biophysics of EMG signal generation. In: Electromyography Physiology Engineering and Noninvasive Applications. Piscataway, NJ: IEEE Press; (2004) 1–26. 10.1002/0471678384.ch1
- Farina D, Merletti R, Stegeman D. Biophysics of the generation of EMG signals. In: Electromyography: Physiology, Engineering, and Noninvasive Applications. Piscataway, NJ: IEEE Press; (2004) 81–105. 10.1002/0471678384.ch4
- Barkhaus PE, Nandedkar SD. EMG evaluation of the motor unit - electrophysiologic biopsy. eMedicine J. (2020).
- Rodriguez-Falces J. Understanding the electrical behavior of the action potential in terms of elementary electrical sources. Adv Physiol Educ. (2015) 39:15–26. 10.1152/advan.00130.2014
- Kleine BU, van Dijk JP, Zwarts MJ, Stegeman DF. Inter-operator agreement in decomposition of motor unit firings from high-density surface EMG. J Electromyogr Kinesiol. (2008) 18:652–61. 10.1016/j.jelekin.2007.01.010
- Holobar A, Farina D, Gazzoni M, Merletti R, Zazula D. Estimating motor unit discharge patterns from high-density surface electromyogram. Clin Neurophysiol. (2009) 120:551–62. 10.1016/j.clinph.2008.10.160
- Nawab SH, Chang S-S, de Luca CJ. High-yield decomposition of surface EMG signals. Clin Neurophysiol. (2010) 121:1602–15. 10.1016/j.clinph.2009.11.092
- de Luca CJ, Adam A, Wotiz R, Gilmore LD, Nawab SH. Decomposition of surface EMG signals. J Neurophysiol. (2006) 96:1646–57. 10.1152/jn.00009.2006
- Drost G, Stegeman DF, van Engelen BG, Zwarts MJ. Clinical applications of high-density surface EMG: a systematic review. J Electromyogr Kinesiol. (2006) 16:586–602. 10.1016/j.jelekin.2006.09.005
- Stegeman DF, Kleine BU, Lapatki BG, van Dijk JP. High-density surface emg: techniques and applications at a motor unit level. Biocybernetics Biomed Eng. (2012) 32:3–27. 10.1016/S0208-5216(12)70039-6
- Farina D, Holobar A. Characterization of human motor units from surface EMG decomposition. Proc IEEE. (2016) 104:353–73. 10.1109/JPROC.2015.2498665
- Besomi M, Hodges P, Clancy EA, van Dieën J, Hug F, Lowery MM, et al. . Consensus for experimental design in electromyography (CEDE) project: amplitude normalization matrix. J Electromyogr Kinesiol. (2020) 53:102438. 10.1016/j.jelekin.2020.102438
- Schwartz MS, Andrasik F. Biofeedback: A Practitioner's Guide. New York, NY: The Guilford Press; (2017).
- Karlsson S, Erlandson B, Gerdle B. A personal computer-based system for real-time analysis of surface EMG signals during static and dynamic contractions. J Electromyogr Kinesiol. (1994) 4:170–80. 10.1016/1050-6411(94)90018-3
- Giggins OM, Persson UM, Caulfield B. Biofeedback in rehabilitation. J Neuroeng Rehabil. (2013) 10:60. 10.1186/1743-0003-10-60
- Akkaya N, Ardic F, Ozgen M, Akkaya S, Sahin F, Kilic A. Efficacy of electromyographic biofeedback and electrical stimulation following arthroscopic partial meniscectomy: a randomized controlled trial. Clin Rehabil. (2012) 26:224–36. 10.1177/0269215511419382
- Gatewood CT, Tran AA, Dragoo JL. The efficacy of post-operative devices following knee arthroscopic surgery: a systematic review. Knee Surg Sports Traumatol Arthrosc. (2017) 25:501–16. 10.1007/s00167-016-4326-4
- Wang AC, Wang Y-Y, Chen M-C. Single-blind, randomized trial of pelvic floor muscle training, biofeedback-assisted pelvic floor muscle training, and electrical stimulation in the management of overactive bladder. Urology. (2004) 63:61–6. 10.1016/j.urology.2003.08.047
- Voorham JC, de Wachter S, van den Bos TW, Putter H, Lycklama à Nijeholt GA, Voorham-van der Zalm PJ. The effect of EMG biofeedback assisted pelvic floor muscle therapy on symptoms of the overactive bladder syndrome in women: a randomized controlled trial. Neurourol Urodyn. (2017) 36:1796–803. 10.1002/nau.23180
- Lal N, Simillis C, Slesser A, Kontovounisios C, Rasheed S, Tekkis PP, et al. . A systematic review of the literature reporting on randomised controlled trials comparing treatments for faecal incontinence in adults. Acta Chir Belg. (2019) 119:1–15. 10.1080/00015458.2018.1549392
- Holtermann A, Mork P, Andersen L, Olsen HB, Søgaard K. The use of EMG biofeedback for learning of selective activation of intra-muscular parts within the serratus anterior muscle: a novel approach for rehabilitation of scapular muscle imbalance. J Electromyogr Kinesiol. (2010) 20:359–65. 10.1016/j.jelekin.2009.02.009
- Ma C, Szeto GP, Yan T, Wu S, Lin C, Li L. Comparing biofeedback with active exercise and passive treatment for the management of work-related neck and shoulder pain: a randomized controlled trial. Arch Phys Med Rehabil. (2011) 92:849–58. 10.1016/j.apmr.2010.12.037
- Neblett R. Surface electromyographic (SEMG) biofeedback for chronic low back pain. Healthcare. (2016) 4:27. 10.3390/healthcare4020027
- Falla DL, Jull GA, Hodges PW. Patients with neck pain demonstrate reduced electromyographic activity of the deep cervical flexor muscles during performance of the craniocervical flexion test. Spine. (2004) 29:2108–14. 10.1097/01.brs.0000141170.89317.0e
- Dursun E, Dursun N, Alican D. Effects of biofeedback treatment on gait in children with cerebral palsy. Disabil Rehabil. (2004) 26:116–20. 10.1080/09638280310001629679
- Stanton R, Ada L, Dean CM, Preston E. Biofeedback improves activities of the lower limb after stroke: a systematic review. J Physiother. (2011) 57:145–55. 10.1016/S1836-9553(11)70035-2
- Hjorth R, Walsh J, Willison R. The distribution and frequency of spontaneous fasciculations in motor neurone disease. J Neurol Sci. (1973) 18:469–74. 10.1016/0022-510X(73)90140-8
- Hogrel J-Y. Use of surface EMG for studying motor unit recruitment during isometric linear force ramp. J Electromyogr Kinesiol. (2003) 13:417–23. 10.1016/S1050-6411(03)00026-9
- de Luca CJ. The use of surface electromyography in biomechanics. J Appl Biomech. (1997) 13:135–63. 10.1123/jab.13.2.135
- McManus L, Hu X, Rymer WZ, Suresh NL, Lowery MM. Motor unit activity during fatiguing isometric muscle contraction in hemispheric stroke survivors. Front Hum Neurosci. (2017) 11:569 10.3389/fnhum.2017.00569
- Nishizono H, Saito Y, Miyashita M. The estimation of conduction velocity in human skeletal muscle in situ with surface electrodes. Electroencephalogr Clin Neurophysiol. (1979) 46:659–64. 10.1016/0013-4694(79)90103-2
- Arendt-Nielsen L, Zwarts M. Measurement of muscle fiber conduction velocity in humans: techniques and applications. J Clin Neurophysiol. (1989) 6:173–90. 10.1097/00004691-198904000-00004
- Farina D, Macaluso A, Ferguson RA, de Vito G. Effect of power, pedal rate, and force on average muscle fiber conduction velocity during cycling. J Appl Physiol. (2004) 97:2035–41. 10.1152/japplphysiol.00606.2004
- Sbriccoli P, Sacchetti M, Felici F, Gizzi L, Lenti M, Scotto A, et al. . Non-invasive assessment of muscle fiber conduction velocity during an incremental maximal cycling test. J Electromyogr Kinesiol. (2009) 19:e380–6. 10.1016/j.jelekin.2009.03.008
- Webber C, Schmidt M, Walsh J. Influence of isometric loading on biceps EMG dynamics as assessed by linear and nonlinear tools. J Appl Physiol. (1995) 78:814–22. 10.1152/jappl.1995.78.3.814
- Richman JS, Moorman JR. Physiological time-series analysis using approximate entropy and sample entropy. Am J Physiol Heart Circ Physiol. (2000) 278:H2039–49. 10.1152/ajpheart.2000.278.6.H2039
- Clancy EA, Farina D, Filligoi G. Single-channel techniques for information extraction from the surface EMG signal. In: Merletti R, Parker P. editors. Electromyography: Physiology, Engineering, and Noninvasive Applications. Piscataway, NJ: Wiley Online Library; (2004) 133–68. 10.1002/0471678384.ch6
- Mesin L, Cescon C, Gazzoni M, Merletti R, Rainoldi A. A bi-dimensional index for the selective assessment of myoelectric manifestations of peripheral and central muscle fatigue. J Electromyogr Kinesiol. (2009) 19:851–63. 10.1016/j.jelekin.2008.08.003
- Farina D, Fattorini L, Felici F, Filligoi G. Nonlinear surface EMG analysis to detect changes of motor unit conduction velocity and synchronization. J Appl Physiol. (2002) 93:1753–63. 10.1152/japplphysiol.00314.2002
- Fattorini L, Felici F, Filligoi G, Traballesi M, Farina D. Influence of high motor unit synchronization levels on non-linear and spectral variables of the surface EMG. J Neurosci Methods. (2005) 143:133–9. 10.1016/j.jneumeth.2004.09.018
- Flood MW, Jensen B, Malling A, Lowery MM. Increased Emg intermuscular coherence and reduced signal complexity in Parkinson's disease. Clin Neurophysiol. (2019) 130, 259–269. 10.1016/j.clinph.2018.10.023
- McManus L, Flood MW, Lowery MM. Beta-band motor unit coherence and nonlinear surface EMG features of the first dorsal interosseous muscle vary with force. J Neurophysiol. (2019) 122:1147–62. 10.1152/jn.00228.2019
- Zwarts M, Stegeman D, van Dijk J. Surface EMG applications in neurology. In: Merletti R, Parker P. editors. Electromyography: Physiology, Engineering, and Noninvasive Applications. Piscataway, NJ: IEEE Press; (2004). 323–42. 10.1002/0471678384.ch12
- Merletti R, Farina D. Surface Electromyography: Physiology, Engineering, and Applications. Piscataway, NJ: IEEE Press; (2016). 10.1002/9781119082934
- Tankisi H, Burke D, Cui L, de Carvalho M, Kuwabara S, Nandedkar SD, et al. . Standards of instrumentation of EMG. Clin Neurophysiol. (2020) 131:243–58. 10.1016/j.clinph.2019.07.025
- Gitter AJ, Stolov WC. AAEM Minimonograph# 16: instrumentation and measurement in electrodiagnostic medicine–Part I. Muscle Nerve. (1995) 18:799–811. 10.1002/mus.880180803
- Gitter AJ, Stolov WC. AAEM Minimonograph# 16: instrumentation and measurement in electrodiagnostic medicine–Part II. Muscle Nerve. (1995) 18:812–24. 10.1002/mus.880180804
- Merletti R, Cerone G. Tutorial. Surface EMG detection, conditioning and pre-processing: best practices. J Electromyogr Kinesiol. (2020) 54:102440. 10.1016/j.jelekin.2020.102440
- Soderberg GL, Knutson LM. A guide for use and interpretation of kinesiologic electromyographic data. Phys Ther. (2000) 80:485–98. 10.1093/ptj/80.5.485
- Besomi M, Hodges PW, van Dieën J, Carson RG, Clancy EA, Disselhorst-Klug C, et al. Consensus for experimental design in electromyography (CEDE) project: electrode selection matrix. J Electromyogr Kinesiol. (2019) 48:128–44. 10.1016/j.jelekin.2019.07.008
- van Dijk J, Lowery M, Lapatki B, Stegeman D. Evidence of potential averaging over the finite surface of a bioelectric surface electrode. Ann Biomed Eng. (2009) 37:1141–51. 10.1007/s10439-009-9680-7
- Perotto AO. Anatomical Guide for the Electromyographer: the Limbs and Trunk. Charles C Thomas Publisher; (2011).
- Lowery MM, Stoykov NS, Kuiken TA. Independence of myoelectric control signals examined using a surface EMG model. IEEE Trans Biomed Eng. (2003) 50:789–93. 10.1109/TBME.2003.812152
- Perry J, Easterday CS, Antonelli DJ. Surface versus intramuscular electrodes for electromyography of superficial and deep muscles. Phys Ther. (1981) 61:7–15. 10.1093/ptj/61.1.7
- Lowery MM, Stoykov NS, Kuiken TA. A simulation study to examine the use of cross-correlation as an estimate of surface EMG cross talk. J Appl Physiol. (2003) 94:1324–34. 10.1152/japplphysiol.00698.2002
- Wu R, Delahunt E, Ditroilo M, Lowery MM, de Vito G. Effect of knee joint angle and contraction intensity on hamstrings coactivation. Med Sci Sports Exerc. (2017) 49:1668–76. 10.1249/MSS.0000000000001273
- Hermens HJ, Freriks B, Disselhorst-Klug C, Rau G. Development of recommendations for SEMG sensors and sensor placement procedures. J Electromyogr Kinesiol. (2000) 10:361–74. 10.1016/S1050-6411(00)00027-4
- Merletti R, Muceli S. Tutorial. surface EMG detection in space and time: best practices. J Electromyogr Kinesiol. (2019) 49:102363. 10.1016/j.jelekin.2019.102363
- Hodges PW. Editorial: consensus for experimental design in electromyography (CEDE) project. J Electromyogr Kinesiol. (2020) 50:102343. 10.1016/j.jelekin.2019.07.013
- Nilsson J, Panizza M, Hallett M. Principles of digital sampling of a physiologic signal. Electroencephalogr Clin Neurophysiol Evoked Potent Sect. (1993) 89:349–58. 10.1016/0168-5597(93)90075-Z
- Merletti R, Migliorini M. Surface EMG electrode noise and contact impedance. In: Proceedings of the Third General SENIAM Workshop Aachen, (Germany: ) (1998).
- Webster JG. Reducing motion artifacts and interference in biopotential recording. IEEE Trans Biomed Eng. (1984) 823–6. 10.1109/TBME.1984.325244
- Tam H, Webster JG. Minimizing electrode motion artifact by skin abrasion. IEEE Trans Biomed Eng. (1977) 24:134–9. 10.1109/TBME.1977.326117
- Piervirgili G, Petracca F, Merletti R. A new method to assess skin treatments for lowering the impedance and noise of individual gelled Ag–AgCl electrodes. Physiol Meas. (2014) 35:2101–18. 10.1088/0967-3334/35/10/2101
- de Luca CJ, Gilmore LD, Kuznetsov M, Roy SH. Filtering the surface EMG signal: Movement artifact and baseline noise contamination. J Biomech. (2010) 43:1573–9. 10.1016/j.jbiomech.2010.01.027
- Clancy EA, Morin EL, Merletti R. Sampling, noise-reduction and amplitude estimation issues in surface electromyography. J Electromyogr Kinesiol. (2002) 12:1–16. 10.1016/S1050-6411(01)00033-5
- Türker KS. Electromyography: some methodological problems and issues. Phys Ther. (1993) 73:698–710. 10.1093/ptj/73.10.698
- Merlo A, Campanini I. Technical aspects of surface electromyography for clinicians. Open Rehabil J. (2010) 3:98–109. 10.2174/1874943701003010098
- Basmajian JV, de Luca C. Muscles Alive. Baltimore, MD: Williams & Wilkins; (1985).
- Merletti R. Standards for Reporting EMG Data (). J Electromyogr Kinesiol. (1999) 9:3–4.
- Zhou P, Lowery MM, Weir RF, Kuiken TA. Elimination of ECG artifacts from myoelectric prosthesis control signals developed by targeted muscle reinnervation. In: 2005 IEEE Engineering in Medicine and Biology 27th Annual Conference. IEEE; (2005). p. 5276–9.
- MacCabee PJ, Hassan NF. AAEM minimonograph# 39: digital filtering: basic concepts and application to evoked potentials. Muscle Nerve. (1992) 15:865–75. 10.1002/mus.880150802
- Lowery MM, O'Malley MJ. Analysis and simulation of changes in EMG amplitude during high-level fatiguing contractions. IEEE Trans Biomed Eng. (2003) 50:1052–62. 10.1109/TBME.2003.816078
- Winkel J, Jørgensen K. Significance of skin temperature changes in surface electromyography. Eur J Appl Physiol Occu Physiol. (1991) 63:345–8. 10.1007/BF00364460
- Mathiassen S, Winkel J, Hägg G. Normalization of surface EMG amplitude from the upper trapezius muscle in ergonomic studies—a review. J Electromyogr Kinesiol. (1995) 5:197–226. 10.1016/1050-6411(94)00014-X
- Merletti R, Lo Conte LR. Surface EMG signal processing during isometric contractions. J Electromyogr Kinesiol. (1997) 7:241–50. 10.1016/S1050-6411(97)00010-2
- Li X, Zhou P, Aruin AS. Teager–Kaiser energy operation of surface EMG improves muscle activity onset detection. Ann Biomed Eng. (2007) 35:1532–8. 10.1007/s10439-007-9320-z
- Flood MW, O'Callaghan B, Lowery M. Gait event detection from accelerometry using the teager-kaiser energy operator. IEEE Trans Biomed Eng. (2019) 67:658–66. 10.1109/TBME.2019.2919394
- O'Callaghan BP, Flood MW, Lowery MM. Application of the Teagar-Kaiser energy operator and wavelet transform for detection of finger tapping contact and release times using accelerometery In: 2019 41st Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC), IEEE; (2019). p. 4596–9. 10.1109/EMBC.2019.8857901
- McManus L, Hu X, Rymer WZ, Suresh NL, Lowery MM. Muscle fatigue increases beta-band coherence between the firing times of simultaneously active motor units in the first dorsal interosseous muscle. J Neurophysiol. (2016) 115:2830–9. 10.1152/jn.00097.2016
- Dewhurst S, Macaluso A, Gizzi L, Felici F, Farina D, de Vito G. Effects of altered muscle temperature on neuromuscular properties in young and older women. Eur J Appl Physiol. (2010) 108:451–8. 10.1007/s00421-009-1245-9
- Solomonow M, Baratta R, Bernardi M, Zhou B, Lu Y, Zhu M, et al. . Surface and wire EMG crosstalk in neighbouring muscles. J Electromyogr Kinesiol. (1994) 4:131–42. 10.1016/1050-6411(94)90014-0
- de la Fuente C, Machado ÁS, Kunzler MR, Carpes FP. Winter school on sEMG signal processing: an initiative to reduce educational gaps and to promote the engagement of physiotherapists and movement scientists with science. Front Neurol. (2020) 11:509. 10.3389/fneur.2020.00509
Source: PubMed