A Neurophysiological Pattern as a Precursor of Work-Related Musculoskeletal Disorders Using EEG Combined with EMG

Colince Meli Segning, Hassan Ezzaidi, Rubens A da Silva, Suzy Ngomo, Colince Meli Segning, Hassan Ezzaidi, Rubens A da Silva, Suzy Ngomo

Abstract

We aimed to determine the neurophysiological pattern that is associated with the development of musculoskeletal pain that is induced by biomechanical constraints. Twelve (12) young healthy volunteers (two females) performed two experimental realistic manual tasks for 30 min each: (1) with the high risk of musculoskeletal pain development and (2) with low risk for pain development. During the tasks, synchronized electroencephalographic (EEG) and electromyography (EMG) signals data were collected, as well as pain scores. Subsequently, two main variables were computed from neurophysiological signals: (1) cortical inhibition as Task-Related Power Increase (TRPI) in beta EEG frequency band (β.TRPI) and (2) muscle variability as Coefficient of Variation (CoV) from EMG signals. A strong effect size was observed for pain measurement under the high risk condition during the last 5 min of the task execution; with muscle fatigue, because the CoV has decreased below 18%. An increase in cortical inhibition (β.TRPI >50%) was observed after the 5th min of the task in both experimental conditions. These results suggest the following neurophysiological pattern-β.TRPI ≥ 50% and CoV ≤ 18%-as a possible indicator to monitor the development of musculoskeletal pain in the shoulder in the context of repeated and prolonged exposure to manual tasks.

Keywords: EEG; EMG; manual task; musculoskeletal disorders; pain; β.TRPI.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Flowchart diagram of offline electroencephalographic (EEG) preprocessing and Task-Related Power Decrease/Increase in beta frequency band (β.TRPD/TRPI estimation in Matlab software.
Figure 2
Figure 2
Flowchart diagram of EMG preprocessing and Coefficient of Variation (CoV) estimation.
Figure 3
Figure 3
Comparison of mean pain score between both experimental task conditions (LR: Low Risk and HR: High risk) across the 30-min time (t0: baseline measure, before starting each task, t5, t10, t15, t20, t25, and t30: at the end of tasks). Significant differences are marked with asterisk: (* p < 0.05, ** p < 0.01, and *** p < 0.001). ES = effect size of conditions on pain intensity.
Figure 4
Figure 4
Comparison of the average of the normalized EMG PSD for all participants between both experimental task conditions (LR: Low Risk and HR: High risk). ∆ indicates the percentage of difference between both experimental task conditions.
Figure 5
Figure 5
Comparison of the muscle variability for all participants between both experimental task conditions (LR: Low Risk and HR: High risk). ∆ represents the percentage of difference between both experimental task conditions.
Figure 6
Figure 6
Comparison of the cortical inhibition of all participants between both experimental task conditions (LR: Low Risk and HR: High risk). ∆ indicates the percentage of difference between both experimental task conditions. *** Indicates statistical differences (p < 0.001).

References

    1. Stock S.F., Delisle A.A., St-Vincent M., Turcot A., Messing K. Enquête Québécoise sur des Conditions de Travail, D’Emploi, de Santé et de Sécurité du Travail (EQCOTESST) Québec—Institut de Recherche Robert-Sauvé en Santé et Sécurité du Travail; Montreal, QC, Canada: 2011. Troubles musculo-squelettique. Chapter 7.
    1. Woolf A.D. Global burden of osteoarthritis and musculoskeletal diseases. BMC Musculoskelet. Disord. 2015;16:S3. doi: 10.1186/1471-2474-16-S1-S3. (In English)
    1. Nordander C., Ohlsson K., Åkesson I., Arvidsson I., Balogh I., Hansson G.Å., Strömberg U., Rittner R., Skerfving S. Risk of musculoskeletal disorders among females and males in repetitive/constrained work. Ergonomics. 2009;52:1226–1239. doi: 10.1080/00140130903056071. (In English)
    1. Mahdavi N., Motamedzade M., Jamshidi A.A., Darvishi E., Moghimbeygi A., Moghadam R.H. Upper trapezius fatigue in carpet weaving: The impact of a repetitive task cycle. Int. J. Occup. Saf. Ergon. JOSE. 2018;24:41–51. doi: 10.1080/10803548.2016.1234706. (In English)
    1. Bilodeau M., Erb M.D., Nichols J.M., Joiner K.L., Weeks J.B. Fatigue of elbow flexor muscles in younger and older adults. Muscle Nerve. 2001;24:98–106. doi: 10.1002/1097-4598(200101)24:1<98::AID-MUS11>;2-D. (In English)
    1. Clark B.C., Manini T.M., The D.J., Doldo N.A., Ploutz-Snyder L.L. Gender differences in skeletal muscle fatigability are related to contraction type and EMG spectral compression. J. Appl. Physiol. 2003;94:2263–2272. doi: 10.1152/japplphysiol.00926.2002. (In English)
    1. Da Silva R.A., Lariviere C., Arsenault A.B., Nadeau S., Plamondon A. The comparison of wavelet- and Fourier-based electromyographic indices of back muscle fatigue during dynamic contractions: Validity and reliability results. Electromyography Clin. Neurophysiol. 2008;48:147–162. (In English)
    1. Da Silva R.A., Vieira E.R., Cabrera M., Altimari L.R., Aguiar A.F., Nowotny A.H., Carvalho A.F., Oliveira M.R. Back muscle fatigue of younger and older adults with and without chronic low back pain using two protocols: A case-control study. J. Electromyogr. Kinesiol. Off. J. Int. Soc. Electrophysiol. Kinesiol. 2015;25:928–936. doi: 10.1016/j.jelekin.2015.10.003. (In English)
    1. Lariviere C., Arsenault A.B., Gravel D., Gagnon D., Loisel P. Evaluation of measurement strategies to increase the reliability of EMG indices to assess back muscle fatigue and recovery. J. Electromyogr. Kinesiol. Off. J. Int. Soc. Electrophysiol. Kinesiol. 2002;12:91–102. doi: 10.1016/S1050-6411(02)00011-1. (In English)
    1. Nasseroleslami B., Lakany H., Conway B.A. EEG signatures of arm isometric exertions in preparation, planning and execution. Neuroimage. 2014;90:1–14. doi: 10.1016/j.neuroimage.2013.12.011. (In English)
    1. Tecchio F., Zappasodi F., Porcaro C., Barbati G., Assenza G., Salustri C., Rossini P.M. High-gamma band activity of primary hand cortical areas: A sensorimotor feedback efficiency index. Neuroimage. 2008;40:256–264. doi: 10.1016/j.neuroimage.2007.11.038. (In English)
    1. Borghuis J., Hof A.L., Lemmink K.A. The importance of sensory-motor control in providing core stability: Implications for measurement and training. Sports Med. 2008;38:893–916. doi: 10.2165/00007256-200838110-00002. (In English)
    1. Neuper C., Wortz M., Pfurtscheller G. ERD/ERS patterns reflecting sensorimotor activation and deactivation. Prog. Brain Res. 2006;159:211–222. (In English)
    1. Pfurtscheller G. Event-Related Desynchronization. Handbook of Electroencephalography and Clinical Neurophysiology. Elsevier BV; Amsterdam, The Netherlands: 1999. Quantification of ERD and ERS in the time domain; pp. 89–105.
    1. Hummel F., Andres F., Altenmüller E., Dichgans J., Gerloff C. Inhibitory control of acquired motor programmes in the human brain. Brain. 2002;125:404–420. doi: 10.1093/brain/awf030.
    1. Hashimoto Y., Ushiba J., Kimura A., Liu M., Tomita Y. Correlation between EEG-EMG coherence during isometric contraction and its imaginary execution. Acta Neurobiol Exp. 2010;70:76–85.
    1. Descatha A., Roquelaure Y., Chastang J.F., Evanoff B., Melchior M., Mariot C., Ha C., Imbernon E., Goldberg M., Leclerc A. Validity of Nordic-style questionnaires in the surveillance of upper-limb work-related musculoskeletal disorders. Scand. J. Work. Environ. Health. 2007;33:58–65. doi: 10.5271/sjweh.1065. (In English)
    1. Descatha A., Roquelaure Y., Chastang J.F., Evanoff B., Cyr D., Leclerc A. Work, a prognosis factor for upper extremity musculoskeletal disorders? Occup Environ. Med. 2009;66:351–352. doi: 10.1136/oem.2008.042630. (In English)
    1. Andersen J.H., Haahr J.P., Frost P. Risk factors for more severe regional musculoskeletal symptoms: A two-year prospective study of a general working population. Arthritis Rheum. 2007;56:1355–1364. doi: 10.1002/art.22513. (In English)
    1. Husemann B., von Mach C.Y., Borsotto D., Zepf K.I., Scharnbacher J. Comparisons of musculoskeletal complaints and data entry between a sitting and a sit-stand workstation paradigm. Hum. Factors. 2009;51:310–320. doi: 10.1177/0018720809338173. (In English)
    1. Sorensen C.J., Johnson M.B., Callaghan J.P., George S.Z., van Dillen L.R. Validity of a paradigm for low back pain symptom development during prolonged standing. Clin. J. Pain. 2015;31:652–659. doi: 10.1097/AJP.0000000000000148. (In English)
    1. Kozak A., Wirth T., Verhamme M., Nienhaus A. Musculoskeletal health, work-related risk factors and preventive measures in hairdressing: A scoping review. J. Occup. Med. Toxicol. 2019;14:1–14. doi: 10.1186/s12995-019-0244-y.
    1. Silverstein B.A., Fine L.J., Armstrong T.J. Hand wrist cumulative trauma disorders in industry. Br. J. Ind. Med. 1986;43:779–784. doi: 10.1136/oem.43.11.779. (In English)
    1. Spielholz P., Silverstein B., Morgan M., Checkoway H., Kaufman J. Comparison of self-report, video observation and direct measurement methods for upper extremity musculoskeletal disorder physical risk factors. Ergonomics. 2001;44:588–613. doi: 10.1080/00140130118050.
    1. Karcioglu O., Topacoglu H., Dikme O., Dikme O. A systematic review of the pain scales in adults: Which to use? Am. J. Emerg. Med. 2018;36:707–714. doi: 10.1016/j.ajem.2018.01.008. (In English)
    1. Stytsenko K., Jablonskis E., Prahm C. Evaluation of consumer EEG device Emotiv EPOC; Proceedings of the MEi CogSci Conference; Ljubljana, Slovenia. 17–18 June 2011.
    1. Kilavik B.E., Zaepffel M., Brovelli A., MacKay W.A., Riehle A. The ups and downs of beta oscillations in sensorimotor cortex. Exp. Neurol. 2013;245:15–26. doi: 10.1016/j.expneurol.2012.09.014. (In English)
    1. Bartur G., Pratt H., Soroker N. Changes in mu and beta amplitude of the EEG during upper limb movement correlate with motor impairment and structural damage in subacute stroke. Clin. Neurophysiol. 2019;130:1644–1651. doi: 10.1016/j.clinph.2019.06.008.
    1. Aboalayon K.A., Almuhammadi W.S., Faezipour M., Aboalayon K.A., Almuhammadi W.S., Faezipour M. 2015 Long Island Systems, Applications and Technology. IEEE; Piscataway, NJ, USA: 2015. A comparison of different machine learning algorithms using single channel EEG signal for classifying human sleep stages; pp. 1–6.
    1. Chen X., Liu A., Chiang J., Wang Z.J., McKeown M.J., Ward R.K. Removing muscle artifacts from EEG data: Multichannel or single-channel techniques? IEEE Sens. J. 2015;16:1986–1997. doi: 10.1109/JSEN.2015.2506982.
    1. Joyce C.A., Gorodnitsky I.F., Kutas M. Automatic removal of eye movement and blink artifacts from EEG data using blind component separation. Psychophysiology. 2004;41:313–325. doi: 10.1111/j.1469-8986.2003.00141.x.
    1. Jiang X., Bian G.-B., Tian Z. Removal of artifacts from EEG signals: A review. Sensors. 2019;19:987. doi: 10.3390/s19050987.
    1. Molina V., Bachiller A., Gomez-Pilar J., Lubeiro A., Hornero R., Cea-Cañas B., Valcárcel C., Haidar M.K., Poza J. Deficit of entropy modulation of the EEG in schizophrenia associated to cognitive performance and symptoms. A replication study. Schizophr. Res. 2018;195:334–342. doi: 10.1016/j.schres.2017.08.057.
    1. Power J.D., Lynch C.J., Dubin M.J., Silver B.M., Martin A., Jones R.M. Characteristics of respiratory measures in young adults scanned at rest, including systematic changes and “missed” deep breaths. Neuroimage. 2020;204:116234. doi: 10.1016/j.neuroimage.2019.116234.
    1. Wang D., Miao D., Blohm G. Multi-class motor imagery EEG decoding for brain-computer interfaces. Front. Neurosci. 2012;6:151. doi: 10.3389/fnins.2012.00151.
    1. Bai Y., Huang G., Tu Y., Tan A., Hung Y.S., Zhang Z. Normalization of pain-evoked neural responses using spontaneous EEG improves the performance of EEG-based cross-individual pain prediction. Front. Comput. Neurosci. 2016;10:31. doi: 10.3389/fncom.2016.00031.
    1. Mangia A.L., Ursino M., Lannocca M., Cappello A. Transcallosal inhibition during motor imagery: Analysis of a neural mass model. Front. Comput. Neurosci. 2017;11:57. doi: 10.3389/fncom.2017.00057.
    1. Al-Nashash H., Tong S., Thakor N.V. Quantitative EEG Analysis Methods and Clinical Applications. Artech House; New York, NY, USA: 2009. Single-channel EEG analysis; pp. 70–126.
    1. Makeig S., Debener S., Onton J., Delorme A. Mining event-related brain dynamics. Trends Cogn. Sci. 2004;8:204–210. doi: 10.1016/j.tics.2004.03.008.
    1. Hatta T., Giambini H., Sukegawa K., Yamanaka Y., Sperling J.W., Steinmann S.P., Itoi E., An K.N. Quantified mechanical properties of the deltoid muscle using the shear wave elastography: Potential implications for reverse shoulder arthroplasty. PLoS ONE. 2016;11:e0155102. doi: 10.1371/journal.pone.0155102.
    1. Boettcher C.E., Ginn K.A., Cathers I. Standard maximum isometric voluntary contraction tests for normalizing shoulder muscle EMG. J. Orthop. Res. Off. Publ. Orthop. Res. 2008;26:1591–1597. doi: 10.1002/jor.20675. (In English)
    1. Kumar D.K., Pah N.D., Bradley A. Wavelet analysis of surface electromyography. IEEE Trans. Neural Syst. Rehabil. Eng. 2003;11:400–406. doi: 10.1109/TNSRE.2003.819901.
    1. Czaprowski D., Afeltowicz A., Gębicka A., Pawłowska P., Kędra A., Barrios C., Hadała M. Abdominal muscle EMG-activity during bridge exercises on stable and unstable surfaces. Phys. Ther. Sport. 2014;15:162–168. doi: 10.1016/j.ptsp.2013.09.003.
    1. Burden A. How should we normalize electromyograms obtained from healthy participants? What we have learned from over 25 years of research. J. Electromyogr. Kinesiol. Off. J. Int. Soc. Electrophysiol. Kinesiol. 2010;20:1023–1035. doi: 10.1016/j.jelekin.2010.07.004. (In English)
    1. Zhang Z., Liu H., Chan S., Luk K., Hu Y. Time-dependent power spectral density estimation of surface electromyography during isometric muscle contraction: Methods and comparisons. J. Electromyogr. Kinesiol. 2010;20:89–101. doi: 10.1016/j.jelekin.2008.09.007.
    1. Terrier P., Schutz Y. Variability of gait patterns during unconstrained walking assessed by satellite positioning (GPS) Eur. J. Appl. Physiol. 2003;90:554–561. doi: 10.1007/s00421-003-0906-3.
    1. Bosch T., Mathiassen S.E., Visser B., Looze M.D., Dieën J.V. The effect of work pace on workload, motor variability and fatigue during simulated light assembly work. Ergonomics. 2011;54:154–168. doi: 10.1080/00140139.2010.538723.
    1. Van Dieën J.H., der Putten E.P.W., Kingma I., de Looze M.P. Low-level activity of the trunk extensor muscles causes electromyographic manifestations of fatigue in absence of decreased oxygenation. J. Electromyogr. Kinesiol. 2009;19:398–406. doi: 10.1016/j.jelekin.2007.11.010.
    1. Madeleine P., Mathiassen S.E., Arendt-Nielsen L. Changes in the degree of motor variability associated with experimental and chronic neck–shoulder pain during a standardised repetitive arm movement. Exp. Brain Res. 2008;185:689–698. doi: 10.1007/s00221-007-1199-2.
    1. Mathiass S., Aminoff T. Motor control and cardiovascular responses during isoelectric contractions of the upper trapezius muscle: Evidence for individual adaptation strategies. Eur. J. Appl. Physiol. Occup. Physiol. 1997;76:434–444. doi: 10.1007/s004210050273.
    1. Cohen J. Statistical Power Analysis for the Behavioral Sciences. Routledge; Abingdon, UK: 2013. Some issues in power analysis; pp. 542–553.
    1. Punnett L., Wegman D.H. Work-related musculoskeletal disorders: The epidemiologic evidence and the debate. J. Electromyogr. Kinesiol. 2004;14:13–23. doi: 10.1016/j.jelekin.2003.09.015.
    1. Page P. Beyond statistical significance: Clinical interpretation of rehabilitation research literature. Int J. Sports Phys. Ther. 2014;9:726–736. (In English)
    1. Srinivasan D., Mathiassen S.E. Motor variability in occupational health and performance. Clin. Biomech. 2012;27:979–993. doi: 10.1016/j.clinbiomech.2012.08.007. (In English)
    1. Zhang F.-R., He L.-H., Wu S.-S., Li J.-Y., Ye K.-P., Sheng W. Quantify work load and muscle functional activation patterns in neck-shoulder muscles of female sewing machine operators using surface electromyogram. Chin. Med. J. 2011;124:3731–3737.
    1. Bohannon R.W. Differentiation of maximal from submaximal static elbow flexor efforts by measurement variability. Am. J. Phys. Med. Rehabil. 1987;66:213–218. doi: 10.1097/00002060-198710000-00001.
    1. Simonsen J.C. Coefficient of variation as a measure of subject effort. Arch. Phys. Med. Rehabil. 1995;76:516–520. doi: 10.1016/S0003-9993(95)80504-4.
    1. Harber P., SooHoo K. Static ergonomic strength testing in evaluating occupational back pain. J. Occup. Med. Off. Publ. Ind. Med. Assoc. 1984;26:877–884. doi: 10.1097/00043764-198412000-00005.
    1. Qin J., Lin J.H., Buchholz B., Xu X. Shoulder muscle fatigue development in young and older female adults during a repetitive manual task. Ergonomics. 2014;57:1201–1212. doi: 10.1080/00140139.2014.914576. (In English)
    1. Cowley J.C., Gates D.H. Influence of remote pain on movement control and muscle endurance during repetitive movements. Exp. Brain Res. 2018;236:2309–2319. doi: 10.1007/s00221-018-5303-6. (In English)
    1. Kaiser V., Bauernfeind G., Kreilinger A., Kaufmann T., Kübler A., Neuper C., Müller-Putz G.R. Cortical effects of user training in a motor imagery based brain–computer interface measured by fNIRS and EEG. NeuroImage. 2014;85:432–444. doi: 10.1016/j.neuroimage.2013.04.097.
    1. Huysmans M., Hoozemans M., van der Beek A., de Looze M., van Dieën J. Fatigue effects on tracking performance and muscle activity. J. Electromyogr. Kinesiol. 2008;18:410–419. doi: 10.1016/j.jelekin.2006.11.003.
    1. Moseley G.L., Hodges P.W. Reduced variability of postural strategy prevents normalization of motor changes induced by back pain: A risk factor for chronic trouble? Behav. Neurosci. 2006;120:474. doi: 10.1037/0735-7044.120.2.474.
    1. Parker R.S., Lewis G.N., Rice D.A., McNair P.J. Is motor cortical excitability altered in people with chronic pain? A systematic review and meta-analysis. Brain Stimul. 2016;9:488–500. doi: 10.1016/j.brs.2016.03.020.
    1. Ngomo S., Mercier C., Bouyer L.J., Savoie A., Roy J.-S. Alterations in central motor representation increase over time in individuals with rotator cuff tendinopathy. Clin. Neurophysiol. 2015;126:365–371. doi: 10.1016/j.clinph.2014.05.035.
    1. Schwenkreis P., Scherens A., Rönnau A.K., Höffken O., Tegenthoff M., Maier C. Cortical disinhibition occurs in chronic neuropathic, but not in chronic nociceptive pain. BMC Neurosci. 2010;11:73. doi: 10.1186/1471-2202-11-73. (In English)
    1. Jodoin M., Rouleau D.M., Bellemare A., Provost C., Larson-Dupuis C., Sandman É., Laflamme G.Y., Benoit B., Leduc S., Levesque M., et al. Moderate to severe acute pain disturbs motor cortex intracortical inhibition and facilitation in orthopedic trauma patients: A TMS study. PLoS ONE. 2020;15:e0226452. doi: 10.1371/journal.pone.0226452. (In English)
    1. Le Pera D., Graven-Nielsen T., Valeriani M., Oliviero A., Di Lazzaro V., Tonali P.A., Arendt-Nielsen L. Inhibition of motor system excitability at cortical and spinal level by tonic muscle pain. Clin. Neurophysiol. 2001;112:1633–1641. doi: 10.1016/S1388-2457(01)00631-9.
    1. Thunberg J., Ljubisavljevic M., Djupsjöbacka M., Johansson H. Effects on the fusimotor-muscle spindle system induced by intramuscular injections of hypertonic saline. Exp. Brain Res. 2002;142:319–326. doi: 10.1007/s00221-001-0941-4.
    1. Graven-Nielsen T., Svensson P., Arendt-Nielsen L. Effects of experimental muscle pain on muscle activity and co-ordination during static and dynamic motor function. Electroencephalogr. Clin. Neurophysiol. Electromyogr. Mot. Control. 1997;105:156–164. doi: 10.1016/S0924-980X(96)96554-6.
    1. Graven-Nielsen T., Lund H., Arendt-Nielsen L., Danneskiold-Samsøe B., Bliddal H. Inhibition of maximal voluntary contraction force by experimental muscle pain: A centrally mediated mechanism. Muscle Nerve Off. J. Am. Assoc. Electrodiagn. Med. 2002;26:708–712. doi: 10.1002/mus.10225.
    1. Greenberg D.L. Evaluation and treatment of shoulder pain. Med. Clin. 2014;98:487–504. doi: 10.1016/j.mcna.2014.01.016.
    1. Luime J., Koes B.W., Hendriksen I.J.M., Burdorf A., Verhagen A.P., Miedema H.S., Verhaar J.A.N. Prevalence and incidence of shoulder pain in the general population; a systematic review. Scand. J. Rheumatol. 2004;33:73–381. doi: 10.1080/03009740310004667.
    1. Crippa M., Torri D., Fogliata L., Belleri L., Alessio L. Implementation of a health education programme in a sample of hairdressing trainees. Med. Lav. 2007;98:48.
    1. Hanvold T.N., Wærsted M., Mengshoel A.M., Bjertness E., Twisk J., Veiersted K.B. A longitudinal study on risk factors for neck and shoulder pain among young adults in the transition from technical school to working life. Scand. J. Work Environ. Health. 2014;40:597–609. doi: 10.5271/sjweh.3437.
    1. Aweto H.A., Tella B.A., Johnson O.Y. Prevalence of work-related musculoskeletal disorders among hairdressers. Int. J. Occup. Med. Environ. Health. 2015;28:545. doi: 10.13075/ijomeh.1896.00291.

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