Electrical activity and fatigue of respiratory and locomotor muscles in obstructive respiratory diseases during field walking test

Jéssica D Cavalcanti, Guilherme Augusto F Fregonezi, Antonio J Sarmento, Thiago Bezerra, Lucien P Gualdi, Francesca Pennati, Andrea Aliverti, Vanessa R Resqueti, Jéssica D Cavalcanti, Guilherme Augusto F Fregonezi, Antonio J Sarmento, Thiago Bezerra, Lucien P Gualdi, Francesca Pennati, Andrea Aliverti, Vanessa R Resqueti

Abstract

Introduction: In subjects with obstructive respiratory diseases the increased work of breathing during exercise can trigger greater recruitment and fatigue of respiratory muscles. Associated with these changes, lower limb muscle dysfunctions, further contribute to exercise limitations. We aimed to assess electrical activity and fatigue of two respiratory and one locomotor muscle during Incremental Shuttle Walking Test (ISWT) in individuals with obstructive respiratory diseases and compare with healthy.

Methods: This is a case-control study. Seventeen individuals with asthma (asthma group) and fifteen with chronic obstructive pulmonary disease (COPD group) were matched with healthy individuals (asthma and COPD control groups). Surface electromyographic (sEMG) activity of sternocleidomastoid (SCM), scalene (ESC), and rectus femoris (RF) were recorded during ISWT. sEMG activity was analyzed in time and frequency domains at baseline and during the test (33%, 66%, and 100% of ISWT total time) to obtain, respectively, signal amplitude and power spectrum density (EMG median frequency [MF], high- and low-frequency bands, and high/low [H/L] ratio).

Results: Asthma group walked a shorter distance than controls (p = 0.0007). sEMG amplitudes of SCM, ESC, and RF of asthma and COPD groups were higher at 33% and 66% of ISWT compared with controls groups (all p<0.05). SCM and ESC of COPD group remained higher until 100% of the test. MF of ESC and RF decreased in asthma group (p = 0.016 and p < 0.0001, respectively) versus controls, whereas MF of SCM (p < 0.0001) decreased in COPD group compared with controls. H/L ratio of RF decreased (p = 0.002) in COPD group versus controls.

Conclusion: Reduced performance is accompanied by increased electromyographic activity of SCM and ESC and activation of RF in individuals with obstructive respiratory diseases during ISWT. These are susceptible to be more pronounced respiratory and peripheral muscle fatigue than healthy subjects during exercise.

Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1. Flowchart selection of participants.
Fig 1. Flowchart selection of participants.
Fig 2
Fig 2
sEMG amplitude of SCM (A and D), ESC (B and E), and RF (C and F) muscles at baseline and during ISWT moments, in Asthma-group (close circles) on upper panel, COPD-group (close triangles) on the lower panel, and their respective control group (open square). § Mann-Whitney Test: difference between groups. *Friedman Test: compared to baseline.
Fig 3
Fig 3
sEMG frequency median of SCM (A and D), ESC (B and E), and RF (C and F) muscles on ISWT, in Asthma-group (close circles) on upper panel and control group (open square) on the lower panel.
Fig 4
Fig 4
sEMG frequency median of SCM (A and D), ESC (B and E), and RF (C and F) muscles on ISWT, in COPD-group (close triangles) on upper panel and control group (open square) on the lower panel.
Fig 5
Fig 5
The high and low frequency bands, and high/low ratio of SCM (A, D, G, J, M and P), ESC (B, E, H, K, N and Q), and RF (C, F, I, O and R) muscles on ISWT, in Asthma-group (close circles) and control group (open square).
Fig 6
Fig 6
The high and low frequency bands, and high/low ratio of SCM (A, D, G, J, M and P), ESC (B, E, H, K, N and Q), and RF (C, F, I, O and R) muscles on ISWT moments, in COPD group (close triangles) and control group (open square).

References

    1. GINA—Global Initiative for Asthma [homepage on the Internet]. Global Strategy for Asthma Management and Prevention, 2020. [Adobe Acrobat document, 209p.] Available in: .
    1. GOLD–Global Initiative for Chronic Obstructive Lung Disease [homepage on the Internet]. Global Strategy for the diagnosis, management, and prevention of Chronic Obstructive Pulmonary Disease, 2021. [Adobe Acrobat document, 152p.] Available in: .
    1. Jolley C.J., Luo Y.M., Steier J., Reilly C., Seymour J., Lunt A., et al.. Neural respiratory drive in healthy subjects and in COPD. Eur Respir J 2009; 33: 289–297. doi: 10.1183/09031936.00093408
    1. Weatherald J., Lougheed M. D., Tailléand C., Garcia G. Mechanisms, measurement and management of exertional dyspnoea in asthma. Eur Respir Rev 2017; 26: 170015. doi: 10.1183/16000617.0015-2017
    1. Duiverman M.L., De Boer E.W.J., Van Eykernc L.A., De Greef M.H.G., Jansen D.F., Wempe J.B., et al.. Respiratory muscle activity and dyspnea during exercise in chronic obstructive pulmonary disease. Respir Physiol & Neurobiol 2009; 167: 195–200. doi: 10.1016/j.resp.2009.04.018
    1. Jolley C.J., Moxham J. A physiological model of patient-reported breathlessness during daily activities in COPD Eur Respir Rev 2009; 18: 112, 66–79. doi: 10.1183/09059180.00000809
    1. Maltais F., Decramer M., Casaburi R., Barreiro E., Burelle Y., et al.. An Official American Thoracic Society/European Respiratory Society Statement: Update on Limb Muscle Dysfunction in Chronic Obstructive Pulmonary Disease. Am J Respir Crit Care Med 2014; 189 (9): 1121–1137. doi: 10.1164/rccm.201402-0373ST
    1. Decramer M., Lacquet L. M., Fagard R., Rogiers P. Corticosteroids contribute to muscle weakness in chronic airflow obstruction. Am J Respir Crit Care Med 1994; 150: 11–16. doi: 10.1164/ajrccm.150.1.8025735
    1. Ramos E., Oliveira L.V.F., Silva A.B., Costa I.P., Corrêa J.C.F., et al.. Peripheral muscle strength and functional capacity in patients with moderate to severe asthma. Multidiscip Resp Med 2015; 10(3): 1–7. doi: 10.1186/2049-6958-10-3
    1. Canuto F.F., Silva S.M., Sampaio L.M.M., Stirbulov R., Corrêa J.C.F. Neurophysiological and functional assessment of patients with difficult-to-control asthma. Rev. Port. Pneumol 2012; 18 (4): 160–165. doi: 10.1016/j.rppneu.2012.02.008
    1. Decramer M., de Bock V., Dom R. Functional and histologic picture of steroid-induced myopathy in chronic obstructive pulmonar disease. Am J Respir Crit Care Med 1996; 153:1958–1964. doi: 10.1164/ajrccm.153.6.8665061
    1. Vermeulen F. Garcia G., Ninane V., Laveneziana P. Activity limitation and exertional dyspnea in adult asthmatic patients: What do we know? Respir Med 2016; 117: 122–130. doi: 10.1016/j.rmed.2016.06.003
    1. Vollestad N.K. Measurement of human muscle fatigue. J. Neurosci. Meth 1997; 74 (2): 219–227. doi: 10.1016/s0165-0270(97)02251-6
    1. Cifrek M., Medved V., Tonković S., Ostojić S. Surface EMG based muscle fatigue evaluation in biomechanics. Clin biomech 2009; 24: 327–340. doi: 10.1016/j.clinbiomech.2009.01.010
    1. Sheel A.W., Boushel R., Dempsey J.A. Competition for blood flow distribution between respiratory and locomotor muscles: implications for muscle fatigue. J Appl Physiol 2018; 125: 820–831. doi: 10.1152/japplphysiol.00189.2018
    1. Dominelli P.B., Archiza B., Ramsook A.H., Mitchell R.A., Peters C.M., et al.. Effects of respiratory muscle work on respiratory and locomotor blood flow during exercise. Exp Physiol 2017; 102.11: 1535–1547. doi: 10.1113/EP086566
    1. Vogiatzis I., Athanasopoulos D., Habazettl H., Aliverti A., Louvaris Z., Cherouveim E., et al.. Intercostal muscle blood flow limitation during exercise in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2010; 182: 1105–1113. doi: 10.1164/rccm.201002-0172OC
    1. American Thoracic Society/European Respiratory Society. ATS/ERS Statement on Respiratory Muscle Testing. Am J Respir Crit Care Med 2002; 166: 518–624. doi: 10.1164/rccm.166.4.518
    1. Ertl P., Kruse A., Tilp M. Detecting fatigue thresholds from electromyographic signals: A systematic review on approaches and methodologies. J Electromyogr Kinesiol 2016; 30: 216–230 doi: 10.1016/j.jelekin.2016.08.002
    1. Moritani T., Muro M. Motor unit activity and surface electromyogram power spectrum during increasing force of contraction. Eur J Appl Physiol. 1987;56(3):260–5. doi: 10.1007/BF00690890
    1. Basmajian J.V., De Luca C.J., 1985. Muscles Alive: Their Function Revealed by Electromyography, fifth ed. Williams and Wilkins, Baltimore.
    1. Mills K.R. Power spectral analysis of electromyogram and compound muscle action potential during muscle fatigue and recovery. J. Physiol. 1982; 326: 401–409. doi: 10.1113/jphysiol.1982.sp014201
    1. Allison G.T., Fujiwara T. The relationship between EMG median frequency and low frequency band amplitude changes at different levels of muscle capacity. Clin biomech (Bristol, Avon) 2002; 17: 464–469. doi: 10.1016/s0268-0033(02)00033-5
    1. Spruit M.A., Singh S.J., Garvey C., ZuWallack R., Nici L., Rochester C., et al.. American Thoracic Society/European Respiratory Society. As Official American Thoracic Society/European Respiratory Society Statement: Key Concepts and Advances in Pulmonary Rehabilitation. Am J Respir Crit Care Med 2013; 188 (8): e13–e64. doi: 10.1164/rccm.201309-1634ST
    1. Miller M.R., Hankinson J., Brusasco V., Burgos F., Casaburi R., Coates A., et al.. American Thoracic Society/European Respiratory Society. Standardisation of spirometry. Eur Respir J 2005; 26: 319–338. doi: 10.1183/09031936.05.00034805
    1. Pereira C.A.C., Sato T., Rodrigues S.C. Novos valores de referência para espirometria forçada em brasileiros adultos de raça branca. J Bras Pneumol 2007; 33(4): 397–406. doi: 10.1590/s1806-37132007000400008
    1. Neder J.A., Andreoni S., Lerario M.C., Nery L.E. Reference values for lung function tests. II. Maximal respiratory pressures and voluntary ventilation. Braz J Med Biol Res 1999; 32(6): 719–727. doi: 10.1590/s0100-879x1999000600007
    1. Araújo P.R.S., Resqueti V.R., Nascimento J., Carvalho L.A., Cavalcanti A.G.L., Silva V.C., et al.. Valores de referência da pressão inspiratória nasal em indivíduos saudáveis no Brasil: estudo multicêntrico. J Bras Pneumol 2012; 38 (6):700–707. doi: 10.1590/s1806-37132012000600004
    1. Singh S.J., Morgan M.D.L., Scott S., Walters D., Hardman A.E. Development of a shuttle walking test of disability in patients with chronic airways obstruction. Thorax 1992; 47: 1019–1024. doi: 10.1136/thx.47.12.1019
    1. Jurgensen S.P., Antunes L.C.O., Tanni S.E., Banov M.C., Lucheta P.A., Bucceroni A.F., et al.. The incremental shuttle walk test in older Brazilian adults. Respiration 2011; 81(3): 223–8. doi: 10.1159/000319037
    1. Hermens H.J., Freriks B., Disselhorst-Klug C., Rau G. Development of recommendations for SEMG sensors and sensor placement procedures. J Electromyogr Kinesiol 2000; 10: 361–374. doi: 10.1016/s1050-6411(00)00027-4
    1. Fallaa D., Dall’Alba P., Rainold A., Merletti R., Jull G. Location of innervation zones of sternocleidomastoid and scalene muscles–a basis for clinical and research electromyography applications. Clin Neurophysiol 2002; 113: 57–63. doi: 10.1016/s1388-2457(01)00708-8
    1. Cunha A. P. N., Marinho P.E.M., Silva T.N.S., França E.E.T., Amorim C., Filho V.C.G., et al.. Efeito do Alongamento sobrea Atividade dos Músculos Inspiratórios na DPOC. Saúde em Revista 2005; 7 (17): 13–19.
    1. SENIAM- Surface ElectroMyoGraphy for the Non-Invasive Assessment of Muscles. [homepage from Internet]. Available in:
    1. Ball N., Scurr J. Electromyography Normalization Methods for High-Velocity Muscle Actions: Review and Recommendations. J Appl Biomech 2013; 29. doi: 10.1123/jab.29.5.600
    1. Camic C.L., Kovacs A.J., Enquist E.A., VanDusseldorp T.A., Hill E.C., Calantoni A.M., et al.. An EMG frequency-based test for estimating the neuromuscular fatigue threshold during cycle ergometry. Eur J Appl Physiol 2010; 108: 337–34. doi: 10.1007/s00421-009-1239-7
    1. Diefenthaeler F., Bini F.F., Vaz M.A. Frequency band analysis of muscle activation during cycling to exhaustion. Rev Bras Cineantropom Desempenho Hum 2012; 14(3):243–253.
    1. Cifrek M., Tonković S., Medved V. Measurement and analysis of surfasse myoelectric signals during fatigued cyclic dynamic contractions. Measurement 2000; 27: 85–92.
    1. Aubier M., Farkas G., De Troyer A., Mozes R., Roussos C. Detection of diaphragmatic fatigue in man by phrenic stimulation. J Applied Physiol 1981; 50: 538–544.
    1. Fritz C.O., Morris P.E., Richler J.J. Effect Size Estimates: Current Use, Calculations, and Interpretation. J Exper Psychol: Gen 2012; 141(1): 2–18.
    1. Tomczak M., Tomczak E. The need to report effect size estimates revisited. An overview of some recommended measures of effect size. Trends Sport Scien 2014; 1(21): 19–25.
    1. Martin J., Powell E., Shore S., Emrich J., Engel L. A. The role of respiratory muscles in the hyperinflation of bronchial asthma. Am. Rev. Respir. Dis. 1980; 121 (3): 441–447. doi: 10.1164/arrd.1980.121.3.441
    1. Reilly C.C., Jolley C.J., Ward K., MacBean V., Moxham J., Rafferty G.F. Neural respiratory drive measured during inspiratory threshold loading and acute hypercapnia in healthy individuals. Exp Physiol 2013; 1190–1198. doi: 10.1113/expphysiol.2012.071415
    1. Aliverti A. The respiratory muscles during Exercise. Breathe 2016. v.12, n. 2.
    1. Konrad P. The ABC of EMG: A pratical introduction to kinesiological electromyography 2006.
    1. O’Donnell D.E., Revill S.M., Webb K.A. Dynamic Hyperinflation and Exercise Intolerance in Chronic Obstructive Pulmonary Disease. Am J Respir Crit Care Med 2001; 164: 770–777. doi: 10.1164/ajrccm.164.5.2012122
    1. Johnson M.A., Polgar J., Weightman D., Appleton D. Data on the distribution of fibre types in thirty-six human muscles. An autopsy study. J Neurolog Scien 1973; 18: 111–129. doi: 10.1016/0022-510x(73)90023-3
    1. Vikne H., Gundersen K., Liestøl K., Maelen J., Vøllestad N. Intermuscular relationship of human muscle fiber type proportions: slow leg muscles predict slow neck muscles. Muscle Nerve 2012; 45: 527–535. doi: 10.1002/mus.22315
    1. Beck T.W., Stock M.S., Defreitas J.M. Shifts in emg spectral power during fatiguing dynamic contractions. AIChE J 2012. doi: 10.1002/aic.12669
    1. Dempsey J.A., Sheel A.W., St Croix C.M., Morgan B.J. Respiratory influences on sympathetic vasomotor outflow in humans. Respir Physiol Neurobiol 2002; 130: 3–20. doi: 10.1016/s0034-5687(01)00327-9

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