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Assessment of the Functional State of Respiratory Muscles: Methodological Aspects and Data Interpretation

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Abstract—The task of this review was to acquaint specialists with the methodical aspects of studies devoted to the function of human respiratory muscles and the most important points in the interpretation of investigation results. The paper discusses specialized aspects in measuring the maximal respiratory pressures, the main principles of the electromyographic techniques, as well as a possible application of the tension–time index calculation in its various modifications to the assessment of the functional state of inspiratory muscles and the determination of their reserve potential in the norm and diseases that generate additional loads on the respiratory muscles. The functional assessment of respiratory muscles is significant for differential diagnostics in some diseases of the bronchopulmonary, neuromuscular, and cardiovascular systems. The analysis of the functional potential contained in the motor apparatus of the external respiratory system may prove to be very useful for specialists in experimental physiology and athletic and rehabilitation medicine.

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REFERENCES

  1. Polkey, M.I. and Moxham, J., Clinical aspects of respiratory muscle dysfunction in the critically ill, Chest, 2001, vol. 119, no. 3, p. 926.

    Article  CAS  PubMed  Google Scholar 

  2. McKenzie, D.K., Butler, J.E., and Gandevia, S.C., Respiratory muscle function and activation in chronic obstructive pulmonary disease, J. Appl. Physiol., 2009, vol. 107, no. 2, p. 621.

    Article  PubMed  Google Scholar 

  3. Charususin, N., Dacha, S., Gosselink, R., et al., Respiratory muscle function and exercise limitation in patients with chronic obstructive pulmonary disease: a review, Expert Rev. Respir. Med., 2018, vol. 12, no. 1, p. 67.

    Article  CAS  PubMed  Google Scholar 

  4. Gea, J., Pascual, S., Casadevall, C., et al., Muscle dysfunction in chronic obstructive pulmonary disease: update on causes and biological findings, J. Thorac. Dis., 2015, vol. 7, no. 10, p. 418.

    Google Scholar 

  5. Barreiro, E. and Gea, J., Respiratory and limb muscle dysfunction in COPD, Int. J. Chronic Obstruct. Pulm. Dis., 2015, vol. 12, p. 413.

    Article  Google Scholar 

  6. Aleksandrova, N.P. and Isaev, G.G., Central and peripheral components of diaphragmatic fatigue during inspiratory resistive load in cats, Acta Physiol Scand., 1997, vol. 161, p. 355.

    Article  CAS  PubMed  Google Scholar 

  7. Segizbaeva, M. and Aleksandrova, N., The effect of oxygen breathing on inspiratory muscle fatigue development during resistive load in cycling men, J. Physiol. Pharmacol., 2009, vol. 60, no. 5, p. 111.

    PubMed  Google Scholar 

  8. Janssens, L., Brumagne, S., McConnell, A.K., et al., The assessment of inspiratory muscle fatigue in healthy individuals: a systematic review, Respir. Med., 2013, vol. 107, no. 3, p. 331.

    Article  PubMed  Google Scholar 

  9. Segizbaeva, M.O. and Aleksandrova, N.P., Inspiratory muscle resistance to fatigue during exercise and simulated airway obstruction, Hum. Physiol., 2014, vol. 40, no. 6, p. 683.

    Article  Google Scholar 

  10. American Thoracic Society/European Respiratory Society, ATS/ERS statement on respiratory muscle testing, Am. J. Respir. Crit. Care Med., 2002, vol. 166, no. 4, p. 518.

  11. Laghi, F. and Tobin, M.J., Disorders of the respiratory muscles, Am. J. Respir. Crit. Care Med., 2003, vol. 168, p. 10.

    Article  PubMed  Google Scholar 

  12. Enright, P.L., Kronmal, R.A., Manolio, T.A., et al., Respiratory muscle strength in the elderly. Correlates and reference values, Am. J. Respir. Crit. Care Med., 1994, vol. 149, p. 430.

    Article  CAS  PubMed  Google Scholar 

  13. Evans, J.A. and Whitelaw, W.A., The assessment of maximal respiratory mouth pressure in adults, Respir. Care, 2009, vol. 54, no. 10, p. 1348.

    PubMed  Google Scholar 

  14. Sclauser Pessoa, I.M., Parreira, V.F., Fregonezi, G.A., et al., Reference values for maximal inspiratory pressure: a systematic review, Can. Respir. J., 2014, vol. 21, no. 1, p. 43.

    Article  PubMed  Google Scholar 

  15. Mellies, U., Stehling, F., and Dohna-Schwake, C., Normal values for inspiratory muscle function in children, Physiol. Meas., 2014, vol. 35, no. 10, p. 1975.

    Article  PubMed  Google Scholar 

  16. Gilbert, R., Peppi, D., and Auchincloss, J.H., Measurement of transdiaphragmatic pressure with a single gastric-esophageal probe, J. Appl. Physiol., 1979, vol. 47, no. 3, p. 628.

    Article  CAS  PubMed  Google Scholar 

  17. Agostoni, T. and Rahn, H., Abdominal and thoracic pressures at different lung volume, J. Appl. Physiol., 1960, vol. 15, no. 6, p. 1087.

    Article  CAS  PubMed  Google Scholar 

  18. Milic-Emili, J., Mead, S., Turner, S.M., and Glaser, E.M., Improved technique for estimating pleural pressure from esophageal balloons, J. Appl. Physiol., 1964, vol. 19, no. 1, p. 207.

    Article  CAS  PubMed  Google Scholar 

  19. Black, L.F. and Hyatt, R.E., Maximal respiratory pressures: normal values and relationship to age and sex, Am. Rev. Respir. Dis., 1969, vol. 99, p. 696.

    CAS  PubMed  Google Scholar 

  20. O’Neill, S. and McCarthy, D.S., Postural relief of dyspnoea in severe chronic airflow limitation: relationship to respiratory muscle strength, Thorax, 1983, vol. 38, no. 8, p. 595.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Heijdra, Y.F., Dekhuijzen, P.N., van Herwaar-den, C.L., and Folgering, H.T., Effects of body position, hyperinflation, and blood gas tensions on maximal respiratory pressures in patients with chronic obstructive pulmonary disease, Thorax, 1994, vol. 49, p. 453.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Costa, R., Almeida, N., Ribeiro, F., et al., Body position influences the maximum inspiratory and expiratory mouth pressures of young healthy subjects, Physiotherapy, 2015, vol. 101, no. 2, p. 239.

    Article  PubMed  Google Scholar 

  23. Segizbaeva, M.O., Pogodin, M.A., and Aleksandrova, N.P., Effects of body positions on respiratory muscle activation during maximal inspiratory maneuvers, Adv. Exp. Med. Biol., 2013, vol. 756, p. 355.

    Article  CAS  PubMed  Google Scholar 

  24. Wohlgemuth, M., van der Kooi, E.L., Hendriks, J.C., et al., Face mask spirometry and respiratory pressures in normal subjects, Eur. Respir. J., 2003, vol. 22, p. 1001.

    Article  CAS  PubMed  Google Scholar 

  25. Troosters, T., Gosselink, R., and Decramer, M., Respiratory muscle assessment, in Lung Function Testing, Gosselink, R. and Stam, H., Eds., Lausanne: Eur. Respir. Soc., 2005, vol. 31, p. 57.

    Google Scholar 

  26. Maillard, J.O., Burdet, L., van Melle, G., and Fitting, J.W., Reproducibility of twitch mouth pressure, sniff nasal inspiratory pressure, and maximal inspiratory pressure, Eur. Respir. J., 1998, vol. 11, p. 901.

    Article  CAS  PubMed  Google Scholar 

  27. Hulzebos, E., Takken, T., Reijneveld, E.A., et al., Reference values for respiratory muscle strength in children and adolescents, Respiration, 2018, vol. 95, no. 4, p. 235.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Choi, W.H., Shin, M.J., Jang, M.H., et al., Maximal inspiratory pressure and maximal expiratory pressure in healthy Korean children, Ann. Rehabil. Med., 2017, vol. 41, no. 2, p. 299.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Hautmann, H., Hefele, S., Schotten, K., and Huber, R.M., Maximal inspiratory mouth pressures (PImax) in healthy subjects—what is the lower limit of normal? Respir. Med., 2000, vol. 94, p. 689.

    Article  CAS  PubMed  Google Scholar 

  30. Harik-Khan, R., Wise, R.A., and Fozard, J.L., Determinants of maximal inspiratory pressure, Am. J. Respir. Crit. Care Med., 1998, vol. 158, no. 5, p. 1459.

    Article  CAS  PubMed  Google Scholar 

  31. Fregonezi, G., Azevedo, I.G., Resqueti, V.R., et al., Muscle impairment in neuromuscular disease using an expiratory/inspiratory pressure ratio, Respir. Care, 2015, vol. 60, no. 4, p. 533.

    Article  PubMed  Google Scholar 

  32. Koo, P., Oyieng’o, D.O., Gartman, E.J., et al., The maximal expiratory-to-inspiratory pressure ratio and supine vital capacity as screening tests for diaphragm dysfunction, Lung, 2017, vol. 195, no. 1, p. 29.

    Article  PubMed  Google Scholar 

  33. Watsford, M.L., Murphy, A.J., Pine, M.J., and Coutts, A.J., The effect of habitual exercise on respiratory-muscle function in older adults, J. Ageing Phys. Act., 2005, vol. 13, no. 1, p. 34.

    Google Scholar 

  34. Chlif, M., Keochkerian, D., Temfemo, A., et al., Inspiratory muscle performance in endurance-trained elderly males during incremental exercise, Respir. Physiol. Neurobiol., 2016, vol. 228, p. 61.

    Article  PubMed  Google Scholar 

  35. McConnell, A.K. and Copestake, A.J., Maximum static respiratory pressures in healthy men and women: issues of reproducibility and interpretation, Respiration, 1999, vol. 66, no. 5, p. 251.

    Article  CAS  PubMed  Google Scholar 

  36. Khemani, R.G., Sekayan, T., Hotz, J., et al., Risk factors for pediatric extubation failure: the importance of respiratory muscle strength, Crit. Care Med., 2017, vol. 45, no. 8, p. e798.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Soori, M., Mohaghegh, S., Hajain, M., and Moraadi, B., Effects of Ramadan fasting on inspiratory muscle function, Asian J. Sports Med., 2016, vol. 7, no. 3, p. e35201.

    Article  PubMed  PubMed Central  Google Scholar 

  38. Chlif, M., Keochkerian, D., Choquet, D., et al., Effects of obesity on breathing pattern, ventilatory neural drive and mechanics, Respir. Physiol. Neurobiol., 2009, vol. 168, no. 3, p. 198.

    Article  PubMed  Google Scholar 

  39. Arena, R. and Cahalin, L.P., Evaluation of cardiorespiratory fitness and respiratory muscle function in the obese population, Prog. Cardiovasc. Dis., 2014, vol. 56, no. 4, p. 457.

    Article  PubMed  Google Scholar 

  40. Segizbaeva, M.O., Donina, Zh.A., Timofeev, N.N., et al., EMG analysis of human inspiratory muscle resistance to fatigue during exercise, Adv. Exp. Med. Biol., 2013, vol. 788, p. 197.

    Article  CAS  PubMed  Google Scholar 

  41. Oueslati, F., Berriri, A., Boone, J., and Ahmaidi, S., Respiratory muscle strength is decreased after maximal incremental exercise in trained runners and cyclists, Respir. Physiol. Neurobiol., 2018, vol. 248, p. 25.

    Article  PubMed  Google Scholar 

  42. Segizbaeva, M.O., Donina, Z.A., Aleksandrov, V.G., and Aleksandrova, N.P., The mechanisms of compensatory responses of the respiratory system to simulated central hypervolemia in normal subjects, in Pulmonary Function, Advances in Experimental Medicine and Biology Series, New York: Springer-Verlag, 2015, vol. 858, p. 9.

    Google Scholar 

  43. Segizbaeva, M.O., Aleksandrova, N.P., Donina, Z.A., et al., Effect of simulated microgravity and Lunar gravity on human inspiratory muscle function: ‘Selena-T’ 2015 study, in Pulmonary Dysfunction and Disease, Advances in Experimental Medicine and Biology Series, New York: Springer-Verlag, 2016, vol. 934, p. 31.

    Google Scholar 

  44. Bellemare, F. and Grassino, A., Evaluation of human diaphragm fatigue, J. Appl. Physiol., 1982, vol. 53, no. 5, p. 1196.

    Article  CAS  PubMed  Google Scholar 

  45. Bellemare, F. and Grassino, A., Effect of pressure and timing of contraction on human diaphragm fatigue, J. Appl. Physiol., 1982, vol. 53, no. 5, p. 1190.

    Article  CAS  PubMed  Google Scholar 

  46. García-Río, F., Mediano, O., Pino, J.M., et al., Noninvasive measurement of the maximum relaxation rate of inspiratory muscles in patients with neuromuscular disorders, Respiration, 2006, vol. 73, no. 4, p. 474.

    Article  PubMed  Google Scholar 

  47. Mancini, D., Henson, D., LaManca, J., and Levine, S., Respiratory muscle function and dyspnea in patients with chronic heart failure, Circulation, 1992, vol. 86, p. 909.

    Article  CAS  PubMed  Google Scholar 

  48. Ceriana, P., Vitacca, M., Carlucci, A., et al., Changes of respiratory mechanics in COPD patients from stable state to acute exacerbations with respiratory failure, Int. J. Chronic Obstruct. Pulm. Dis., 2017, vol. 14, no. 2, p. 150.

    Article  Google Scholar 

  49. Hayot, M., Ramonatxo, M., Matecki, S., et al., Noninvasive assessment of inspiratory muscle function during exercise, Am. J. Respir. Crit. Care Med., 2000, vol. 162, no. 6, p. 2201.

    Article  CAS  PubMed  Google Scholar 

  50. Ramonatxo, M., Boulard, P., and Prefaut, C., Validation of a non-invasive tension-time index of inspiratory muscles, J. Appl. Physiol., 1995, vol. 78, no. 2, p. 646.

    Article  CAS  PubMed  Google Scholar 

  51. Gaultier, C., Boule, M., Tournier, G., and Girard, F., Inspiratory force reserve of the respiratory muscles in children with chronic obstructive pulmonary diseases, Am. Rev. Respir. Dis., 1985, vol. 131, no. 6, p. 811.

    CAS  PubMed  Google Scholar 

  52. Gonzalez, C., Servera, E., Celli, B., et al., A simple noninvasive pressure-time index at the mouth to measure respiratory load during acute exacerbation of COPD. A comparison with normal volunteers, Respir. Med., 2003, vol. 97, no. 4. p. 415.

    Article  CAS  PubMed  Google Scholar 

  53. DeTorres, J.P., Talamo, C., Aguirre-Jaime, A., et al., Electromyographic validation of the mouth pressure-time index: a noninvasive assessment of inspiratory muscle load, Respir. Med., 2003, vol. 97, no. 9, p. 1006.

    Article  Google Scholar 

  54. Hayot, M., Perrigault, P.F., Gautier-Dechaud, V., et al., Tension-time index of inspiratory muscles in COPD patients: role of airway obstruction, Respir. Med., 1998, vol. 92, no. 6, p. 828.

    Article  CAS  PubMed  Google Scholar 

  55. Hahn, A., Ankermann, T., Claass, A., et al., Non-invasive tension-time index in relation to severity of disease in children with cystic fibrosis, Pediatr. Pulmonol., 2008, vol. 43, no. 10, p. 973.

    Article  PubMed  Google Scholar 

  56. Hayot, M., Guillaumont, S., Ramonatxo, M., et al., Determinants of the tension-time index of inspiratory muscles in children with cystic fibrosis, Pediatr Pulmonol., 1997, vol. 23, no. 5, p. 336.

    Article  CAS  PubMed  Google Scholar 

  57. Vibarel, N., Hayot, M., and Pellenc, P.M., Noninvasive assessment of inspiratory muscle performance during exercise in patients with chronic heart failure, Eur. Heart J., 1998, vol. 19, no. 5, p. 766.

    Article  CAS  PubMed  Google Scholar 

  58. Mancini, D.M., Ferraro, N., Nazzaro, D., et al., Respiratory muscle deoxygenation during exercise in patients with heart failure demonstrated with near-infrared spectroscopy, J. Am. Coll. Cardiol., 1991, vol. 18, no. 2, p. 492.

    Article  CAS  PubMed  Google Scholar 

  59. Mancini, D.M., Henson, D., LaManca, J., and Levine, S., Respiratory muscle function and dyspnea in patients with chronic congestive heart failure, Circulation, 1992, vol. 86, no. 3, p. 909.

    Article  CAS  PubMed  Google Scholar 

  60. Mulreany, L.T., Weiner, D.J., McDonough, J.M., et al., Noninvasive measurement of the tension-time index in children with neuromuscular disease, J. Appl. Physiol., 2003, vol. 95, no. 3, p. 931.

    Article  PubMed  Google Scholar 

  61. Stehling, F., Alfen, K., Dohna-Schwake, C., and Mellies, U., Respiratory muscle weakness and respiratory failure in pediatric neuromuscular disorders: the value of noninvasive determined tension-time index, Neuropediatrics, 2016, vol. 47, no. 6, p. 374.

    Article  PubMed  Google Scholar 

  62. Hahn, A., Duisberg, B., Neubauer, B.A., et al., Noninvasive determination of the tension-time index in Duchenne muscular dystrophy, Am. J. Phys. Med. Rehabil., 2009, vol. 88, no. 4, p. 322.

    Article  PubMed  Google Scholar 

  63. Chlif, M., Keochkerian, D., Mourlhon, C., et al., Noninvasive assessment of the time-tension index of inspiratory muscles at rest in obese male subjects, Int. J. Obes. (London), 2005, vol. 29, no. 12, p. 1478.

    Article  CAS  Google Scholar 

  64. Currie, A., Patel, D.S., Rafferty, G.F., and Greenough, A., Prediction of exturbation outcome in infants using the tension-time index, Arch. Dis. Child. Fetal Neonatal. Ed., 2011, vol. 96, no. 4, p. 265.

    Article  Google Scholar 

  65. Harikumar, G., Egberongbe, Y., Nadel, S., et al., Tension-time index as a predictor of extubation outcome in ventilated children, Am. J. Respir. Crit. Care Med., 2009, vol. 180, no. 10, p. 982.

    Article  PubMed  PubMed Central  Google Scholar 

  66. McKenzie, D.K. and Gandevia, S.C., Phrenic nerve conduction times and twitch pressures of the human diaphragm, J. Appl. Physiol., 1985, vol. 58, no. 5, p. 1496.

    Article  CAS  PubMed  Google Scholar 

  67. Schweitzer, T.W., Fitzgerald, J.W., Bowden, J.A., and Lynne-Davies, P., Spectral analyses of human inspiratory diaphragmatic electromyograms, J. Appl. Physiol., 1979, vol. 46, p. 152.

    Article  CAS  PubMed  Google Scholar 

  68. Gross, D., Grassino, A., Ross, W.R.D., and Macklem, P.T., Electromyogram pattern of diaphragmatic fatigue, J. Appl. Physiol., 1979, vol. 46, no. 1, p. 1.

    Article  CAS  PubMed  Google Scholar 

  69. Segizbaeva, M.O., Timofeev, N.N., Donina, Zh.A., et al., Effects of inspiratory muscle training on resistance to fatigue of respiratory muscles during exhaustive exercise, in Body Metabolism and Exercise, Advances in Experimental Medicine and Biology Series, New York: Springer-Verlag, 2015, vol. 840, no. 9, p. 35.

  70. HajGhanbari, B., Yamabayashi, C., Buna, T.R., et al., Effects of respiratory muscle training on performance in athletes: a systematic review with meta-analyses, J. Strength Cond. Res., 2013, vol. 27, no. 6, p. 1643.

  71. Vašíčková, J., Neumannová, K., and Svozil, Z., The effect of respiratory muscle training on fin-swimmers’ performance, J. Sports Sci. Med., 2017, vol. 116, no. 4, p. 521.

    Google Scholar 

  72. Mehani, S.H.M., Comparative study of two different respiratory training protocols in elderly patients with chronic obstructive pulmonary disease, Clin. Interventions Aging, 2017, vol. 12, p. 1705.

    Article  Google Scholar 

  73. Menezes, K.K., Nascimento, L.R., Ada, L., et al., Respiratory muscle training increases respiratory muscle strength and reduces respiratory complications after stroke: a systematic review, J. Physiother., 2016, vol. 62, no. 3, p. 138.

    Article  PubMed  Google Scholar 

  74. Human, A., Corten, L., Jelsma, J., and Morrow, B., Inspiratory muscle training for children and adolescents with neuromuscular diseases: a systematic review, Neuromuscular Disord., 2017, vol. 27, no. 6, p. 503.

    Article  Google Scholar 

  75. Neves, L.F., Reis, M.H., Plentz, R.D., et al., Expiratory and expiratory plus inspiratory muscle training improve respiratory muscle strength in subjects with COPD: systematic review, Respir. Care, 2014, vol. 59, no. 9, p. 1381.

    Article  PubMed  Google Scholar 

  76. Sales, A.T., Fregonezi, G.A., Ramsook, A.H., et al., Respiratory muscle endurance after training in athletes and non-athletes: a systematic review and meta-analysis, Phys. Ther. Sport, 2016, vol. 17, p. 76.

    Article  PubMed  Google Scholar 

  77. Yoo, H.J. and Pyun, S.B., Efficacy of bedside respiratory muscle training in patients with stroke: a randomized controlled trial, Am. J. Phys. Med. Rehabil., 2018, vol. 97, no. 10, p. 691.

    Article  PubMed  Google Scholar 

  78. Chlif, M., Keochkerian, D., Feki, Y., et al., Inspiratory muscle activity during incremental exercise in obese men, Int. J. Obes. (London), 2007, vol. 31, no. 9, p. 1456.

    Article  CAS  Google Scholar 

  79. Chlif, M., Chaouachi, A., and Ahmaidi, S., Effect of aerobic exercise training on ventilatory efficiency and respiratory drive in obese subjects, Resp. Care, 2017, vol. 62, no. 7, p. 93.

    Google Scholar 

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ACKNOWLEDGMENTS COMPLIANCE WITH ETHICAL STANDARDS

This study was supported by the Program for Basic Research of State Academies for 2013–2020 (GP-14, chapter 65).

The authors declare that they have no conflict of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.

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  1. Pavlov Institute of Physiology, Russian Academy of Sciences, St. Petersburg, Russia

    M. O. Segizbaeva & N. P. Aleksandrova

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  1. M. O. Segizbaeva
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Segizbaeva, M.O., Aleksandrova, N.P. Assessment of the Functional State of Respiratory Muscles: Methodological Aspects and Data Interpretation. Hum Physiol 45, 213–224 (2019). https://doi.org/10.1134/S0362119719010110

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