Effect of expiratory loaded breathing during moderate exercise on intercostal muscle oxygenation

Abstract

Background: In patients with obstructive lung disease, maintaining adequate ventilation during exercise may require greater contraction of the respiratory muscles, which may lead to a compression of muscle capillaries. Furthermore, dynamic hyperinflation (DH) is frequent during exercise in these patients, as it allows to reach higher expiratory flows and to satisfy respiratory demand. However, in such situation, intercostal muscles are likely to be stretched, which could affect the diameter of their capillaries. Thus, in a context of high level of expiratory resistance, intercostal muscle oxygenation may be disturbed during exercise, especially if DH occurs.
Methods: Twelve participants (22±2 years) performed two sessions of moderate exercise (20 min) by breathing freely with and without a 20-cmH2O expiratory threshold load (ETL). Tissue saturation index (TSI) and concentration changes from rest (∆) in oxygenated ([O2Hb]) and total haemoglobin ([tHb]) were measured in the seventh intercostal space using near-infrared spectroscopy. Respiratory, metabolic and cardiac variables were likewise recorded.
Results: Throughout exercise, dyspnea was higher and TSI was lower in ETL condition than in control (p<0.01). After a few minutes of exercise, ∆ [O2Hb] was also lower in ETL condition, as well as ∆ [tHb], when inspiratory capacity started to be reduced (p<0.05). Changes in [O2Hb] and dyspnea were correlated with changes in expiratory flow rate (Vt/Te) (r = -0.66 and 0.66. respectively; p<0.05).
Conclusion: During exercise with ETL, impaired muscle oxygenation could be due to a limited increase in blood volume resulting from strong muscle contraction and/or occurrence of DH.

Dimensions

Altmetric

PlumX Metrics

Downloads

Download data is not yet available.

References

Heikkinen SAM, Quansah R, Jaakkola JJK, Jaakkola MS. Effects of regular exercise on adult asthma. Eur J Epidemiol 2012;27:397-407. DOI: https://doi.org/10.1007/s10654-012-9684-8

Paneroni M, Simonelli C, Vitacca M, Ambrosino N. Aerobic exercise training in very severe chronic obstructive pulmonary disease: a systematic review and meta-analysis. Am J Phys Med Rehabil 2017;96:541-8. DOI: https://doi.org/10.1097/PHM.0000000000000667

Vogiatzis I, Zakynthinos S. Factors limiting exercise tolerance in chronic lung diseases. In: Terjung R, editor. Comprehensive physiology. Hoboken: J. Wiley & Sons; 2012. Available from: http://doi.wiley.com/10.1002/cphy.c110015 DOI: https://doi.org/10.1002/cphy.c110015

Tantucci C. Expiratory flow limitation definition, mechanisms, methods, and significance. Pulm Med 2013;2013:1–6. DOI: https://doi.org/10.1155/2013/749860

O’Donnell DE, Revill SM, Webb KA. Dynamic hyperinflation and exercise intolerance in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2001;164:770–7. DOI: https://doi.org/10.1164/ajrccm.164.5.2012122

O’Donnell DE, Guenette JA, Maltais F, Webb KA. Decline of resting inspiratory capacity in COPD. Chest 2012;141:753–62. DOI: https://doi.org/10.1378/chest.11-0787

Sliwinski P, Kaminski D, Zielinski J, Yan S. Partitioning of the elastic work of inspiration in patients with COPD during exercise. Eur Respir J 1998;11:416–21. DOI: https://doi.org/10.1183/09031936.98.11020416

Chen S, Li Y, Zheng Z, Luo Q, Chen R. The analysis of components that lead to increased work of breathing in chronic obstructive pulmonary disease patients. J Thorac Dis 2016;8:2212–8. DOI: https://doi.org/10.21037/jtd.2016.08.01

O’Donnell DE, Bertley JC, Chau LK, Webb KA. Qualitative aspects of exertional breathlessness in chronic airflow limitation: pathophysiologic mechanisms. Am J Respir Crit Care Med 1997;155:109–15. DOI: https://doi.org/10.1164/ajrccm.155.1.9001298

O’Donnell DE, Laveneziana P. Dyspnea and activity limitation in COPD: mechanical factors. COPD 2007;4:225–36. DOI: https://doi.org/10.1080/15412550701480455

Laveneziana P, Webb KA, Wadell K, Neder JA, O’Donnell DE. Does expiratory muscle activity influence dynamic hyperinflation and exertional dyspnea in COPD? Respir Physiol Neurobiol 2014;199:24–33. DOI: https://doi.org/10.1016/j.resp.2014.04.005

Faisal A, Alghamdi BJ, Ciavaglia CE, Elbehairy AF, Webb KA, Ora J, et al. Common mechanisms of dyspnea in chronic interstitial and obstructive lung disorders. Am J Respir Crit Care Med 2016;193:299–309. DOI: https://doi.org/10.1164/rccm.201504-0841OC

Wilson TA, Legrand A, Gevenois P-A, De Troyer A. Respiratory effects of the external and internal intercostal muscles in humans. J Physiol 2001;530:319–30. DOI: https://doi.org/10.1111/j.1469-7793.2001.0319l.x

Leenaerts P, Decramer M. Respiratory changes in parasternal intercostal intramuscular pressure. J Appl Physiol 1990 1;68:868–75. DOI: https://doi.org/10.1152/jappl.1990.68.3.868

Poole DC, Musch TI, Kindig CA. In vivo microvascular structural and functional consequences of muscle length changes. Am J Physiol-Heart Circ Physiol 1997;272:2107–14. DOI: https://doi.org/10.1152/ajpheart.1997.272.5.H2107

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;182:1105–13. DOI: https://doi.org/10.1164/rccm.201002-0172OC

Athanasopoulos D, Louvaris Z, Cherouveim E, Andrianopoulos V, Roussos C, Zakynthinos S, et al. Expiratory muscle loading increases intercostal muscle blood flow during leg exercise in healthy humans. J Appl Physiol 2010;109:388–95. DOI: https://doi.org/10.1152/japplphysiol.01290.2009

Quanjer PH, Stanojevic S, Cole TJ, Baur X, Hall GL, Culver BH, et al. Multi-ethnic reference values for spirometry for the 3–95-yr age range: the global lung function 2012 equations. Eur Respir J 2012;40:1324–43. DOI: https://doi.org/10.1183/09031936.00080312

Grassi B, Quaresima V. Near-infrared spectroscopy and skeletal muscle oxidative function in vivo in health and disease: a review from an exercise physiology perspective. J Biomed Opt 2016;21:091313. DOI: https://doi.org/10.1117/1.JBO.21.9.091313

Roy S, McCrory J. Validation of maximal heart rate prediction equations based on sex and physical activity status. Int J Exerc Sci 2015;8:318–30.

Miller MR, Hankinson J, Brusasco V, Burgos F, Casaburi R, Coates A, et al. Standardisation of spirometry. Eur Respir J 2005;26:319–38. DOI: https://doi.org/10.1183/09031936.05.00034805

Johnson BD, Weisman IM, Zeballos RJ, Beck KC. Emerging concepts in the evaluation of ventilatory limitation during exercise. Chest 1999;116:488–503. DOI: https://doi.org/10.1378/chest.116.2.488

Yan S, Kaminski D, Sliwinski P. Reliability of inspiratory capacity for estimating end-expiratory lung volume changes during exercise in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 1997;156:55–9. DOI: https://doi.org/10.1164/ajrccm.156.1.9608113

Guenette JA, Chin RC, Cory JM, Webb KA, O’Donnell DE. Inspiratory capacity during exercise: measurement, analysis, and interpretation. Pulm Med.2013;2013:1–13. DOI: https://doi.org/10.1155/2013/956081

de Bisschop C, Beloka S, Groepenhoff H, van der Plas MN, Overbeek MJ, Naeije R, et al. Is there a competition for oxygen availability between respiratory and limb muscles? Respir Physiol Neurobiol 2014;196:8–16. DOI: https://doi.org/10.1016/j.resp.2014.02.011

Bretonneau Q, Pichon A, de Bisschop C. Intercostal muscle oxygenation during expiratory load breathing at rest. Respir Physiol Neurobiol 2019;261:24–30. DOI: https://doi.org/10.1016/j.resp.2018.12.007

Chance B, Dait MT, Zhang C, Hamaoka T, Hagerman F. Recovery from exercise-induced desaturation in the quadriceps muscles of elite competitive rowers. Am J Physiol-Cell Physiol 1992;262:766–75. DOI: https://doi.org/10.1152/ajpcell.1992.262.3.C766

van Beekvelt MCP, van Engelen BGM, Wevers RA, Colier WNJM. In vivo quantitative near-infrared spectroscopy in skeletal muscle during incremental isometric handgrip exercise. Clin Physiol Funct Imaging 2002;22:210–7. DOI: https://doi.org/10.1046/j.1475-097X.2002.00420.x

Kendrick KR, Baxi SC, Smith RM. Usefulness of the modified 0-10 Borg scale in assessing the degree of dyspnea in patients with COPD and asthma. J Emerg Nurs 2000;26:216–22. DOI: https://doi.org/10.1016/S0099-1767(00)90093-X

Vogiatzis I, Habazettl H, Aliverti A, Athanasopoulos D, Louvaris Z, LoMauro A, et al. Effect of helium breathing on intercostal and quadriceps muscle blood flow during exercise in COPD patients. Am J Physiol-Regul Integr Comp Physiol 2011;300:1549–59. DOI: https://doi.org/10.1152/ajpregu.00671.2010

Aliverti A, Dellacà RL, Lotti P, Bertini S, Duranti R, Scano G, et al. Influence of expiratory flow-limitation during exercise on systemic oxygen delivery in humans. Eur J Appl Physiol 2005;95:229–42. DOI: https://doi.org/10.1007/s00421-005-1386-4

Nieman GF, Paskanik AM, Bredenberg CE. Effect of positive end-expiratory pressure on alveolar capillary perfusion. J Thorac Cardiovasc Surg 1988;95:712–6. DOI: https://doi.org/10.1016/S0022-5223(19)35741-1

Ferrari M, Muthalib M, Quaresima V. The use of near-infrared spectroscopy in understanding skeletal muscle physiology: recent developments. Philos Trans R Soc Math Phys Eng Sci 2011;369:4577–90. DOI: https://doi.org/10.1098/rsta.2011.0230

Stark-Leyva KN, Beck KC, Johnson BD. Influence of expiratory loading and hyperinflation on cardiac output during exercise. J Appl Physiol 2004;96:1920–7. DOI: https://doi.org/10.1152/japplphysiol.00756.2003

Braun NM, Arora NS, Rochester DF. Force-length relationship of the normal human diaphragm. J Appl Physiol 1982;53:405–12. DOI: https://doi.org/10.1152/jappl.1982.53.2.405

DiMarco AF, Romaniuk JR, Supinski G, Kowalski KE. Effects of lung volume on parasternal pressure-generating capacity in dogs. Exp Physiol 2000;85:331–7. DOI: https://doi.org/10.1111/j.1469-445X.2000.01921.x

O’Donnell DE, Ora J, Webb KA, Laveneziana P, Jensen D. Mechanisms of activity-related dyspnea in pulmonary diseases. Respir Physiol Neurobiol 2009;167:116–32. DOI: https://doi.org/10.1016/j.resp.2009.01.010

Aliverti A, Stevenson N, Dellaca RL, Lo Mauro A, Pedotti A, Calverley PMA. Regional chest wall volumes during exercise in chronic obstructive pulmonary disease. Thorax 2004;59:210–6. DOI: https://doi.org/10.1136/thorax.2003.011494

Guenette JA, Webb KA, O’Donnell DE. Does dynamic hyperinflation contribute to dyspnoea during exercise in patients with COPD? Eur Respir J 2012;40:322–9. DOI: https://doi.org/10.1183/09031936.00157711

Kayser B, Sliwinski P, Yan S, Tobiasz M, Macklem PT. Respiratory effort sensation during exercise with induced expiratory-flow limitation in healthy humans. J Appl Physiol 1997;83:936–47. DOI: https://doi.org/10.1152/jappl.1997.83.3.936

De Troyer A, Gorman RB, Gandevia SC. Distribution of inspiratory drive to the external intercostal muscles in humans. J Physiol 2003;546:943–54. DOI: https://doi.org/10.1113/jphysiol.2002.028696

Stubbing DG, Pengelly LD, Morse JL, Jones NL. Pulmonary mechanics during exercise in normal males. J Appl Physiol 1980;49:506–10. DOI: https://doi.org/10.1152/jappl.1980.49.3.506

Stubbing DG, Pengelly LD, Morse JL, Jones NL. Pulmonary mechanics during exercise in subjects with chronic airflow obstruction. J Appl Physiol 1980;49:511–5. DOI: https://doi.org/10.1152/jappl.1980.49.3.511

Johnson BD, Scanlon PD, Beck KC. Regulation of ventilatory capacity during exercise in asthmatics. J Appl Physiol 1995;79:892–901. DOI: https://doi.org/10.1152/jappl.1995.79.3.892

de Bisschop C, Montaudon M, Glénet S, Guénard H. Feasibility of intercostal blood flow measurement by echo-Doppler technique in healthy subjects. Clin Physiol Funct Imaging 2017;37:282–7. DOI: https://doi.org/10.1111/cpf.12298

Aliverti A, Iandelli I, Duranti R, Cala SJ, Kayser B, Kelly S, et al. Respiratory muscle dynamics and control during exercise with externally imposed expiratory flow limitation. J Appl Physiol 2002;92:1953–63. DOI: https://doi.org/10.1152/japplphysiol.01222.2000

Bougault V, Lonsdorfer-Wolf E, Charloux A, Richard R, Geny B, Oswald-Mammosser M. Does thoracic bioimpedance accurately determine cardiac output in COPD patients during maximal or intermittent exercise? Chest 2005;127:1122–31. DOI: https://doi.org/10.1016/S0012-3692(15)34456-1

Lalande S, Luoma CE, Miller AD, Johnson BD. Expiratory loading improves cardiac output during exercise in heart failure. Med Sci Sports Exerc 2012;44:2309–14. DOI: https://doi.org/10.1249/MSS.0b013e318267bb5a

Hartman JE, Boezen HM, Zuidema MJ, de Greef MHG, ten Hacken NHT. Physical activity recommendations in patients with chronic obstructive pulmonary disease. Respiration 2014;88:92–100. DOI: https://doi.org/10.1159/000360298

Gloeckl R, Marinov B, Pitta F. Practical recommendations for exercise training in patients with COPD. Eur Respir Rev 2013;22:178–86. DOI: https://doi.org/10.1183/09059180.00000513

Published
2020-10-26
Info
Issue
Section
Original Research Articles
Keywords:
Intercostal muscle oxygenation, NIRS, expiratory threshold load, exercise, dynamic hyperinflation
Statistics
  • Abstract views: 904

  • PDF: 98
  • HTML: 0
How to Cite
Bretonneau, Q., Pichon, A., & de Bisschop, C. (2020). Effect of expiratory loaded breathing during moderate exercise on intercostal muscle oxygenation. Multidisciplinary Respiratory Medicine, 15. https://doi.org/10.4081/mrm.2020.702