Clinical Evaluation of Dyspnoea in Obstructive Lung Disease – Progressing from Psychometrics to Physiology
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Feb 27, 2024
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Abstract
Dyspnoea is a common symptom that afflicts persons with myriad medical conditions. Among sufferers of lung disorders such as chronic obstructive pulmonary disease, dyspnoea, together with effort intolerance, are the major complaints. Dyspnoea is a marker of disease severity and adverse prognosis of chronic obstructive pulmonary disease, and the need for symptom alleviation in improving health status is ever-present, but the quantification of this symptom is challenging in clinical practice, and is mostly limited to the use of questionnaires and self-reports currently. Numerous psychometric tools have been developed to measure the severity of dyspnoea clinically, but their utility is vitiated by the complexity and multidimensional nature of the symptom. The lack of a universally accepted and accurate measurement tool is likely to hinder future progress in developing novel treatments for relieving dyspnoea.
Physiological measurements have been used to complement or supplant psychometric evaluation of dyspnoea but simple stationary lung function tests do not correlate sufficiently well with dyspnoea severity in patients with chronic obstructive pulmonary disease, while complex exercise testing is impractical or limited to specialized research labs. In recent years, the use of non-invasive surface electromyography of the diaphragm and/or accessory muscles of respiration is gaining attention as a promising physiological assessment of dyspnoea with potential for widespread clinical applications. Although substantial technological gaps still exist between bench and bedside, the current interest, as evidenced by the number of med-tech collaborations in surface respiratory electromyography, appears to be well justified. This review aims to summarize the past and present methodologies as well as future developments in evaluating and quantifying dyspnoea, especially in patients with chronic obstructive pulmonary disease.
Article Details
How to Cite
ONG, Kian Chung.
Clinical Evaluation of Dyspnoea in Obstructive Lung Disease – Progressing from Psychometrics to Physiology.
Medical Research Archives, [S.l.], v. 12, n. 2, feb. 2024.
ISSN 2375-1924.
Available at: <https://esmed.org/MRA/mra/article/view/5019>. Date accessed: 27 apr. 2024.
doi: https://doi.org/10.18103/mra.v12i2.5019.
Section
Research Articles
The Medical Research Archives grants authors the right to publish and reproduce the unrevised contribution in whole or in part at any time and in any form for any scholarly non-commercial purpose with the condition that all publications of the contribution include a full citation to the journal as published by the Medical Research Archives.
References
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2. Dyspnea. Mechanisms, assessment, and management: a consensus statement. American Thoracic Society. Am J Respir Crit Care Med. 1999;159(1):321-340.
3. Parshall MB, Schwartzstein RM, Adams L, et al. An official American Thoracic Society statement: update on the mechanisms, assessment, and management of dyspnea. Am J Respir Crit Care Med. 2012;185(4):435-452.
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5. O'Donnell DE, Milne KM, James MD, de Torres JP, Neder JA. Dyspnea in COPD: New Mechanistic Insights and Management Implications. Adv Ther. 2020;37(1):41-60.
6. Hanania NA, O'Donnell DE. Activity-related dyspnea in chronic obstructive pulmonary disease: physical and psychological consequences, unmet needs, and future directions. Int J Chron Obstruct Pulmon Dis. 2019;14:1127-1138.
7. Ong KC. Evaluating dyspnoea in chronic obstructive pulmonary disease. Precision and Future Medicine 2021;5(2):62-68.
8. O’Donnell DE, Banzett RB, Carrieri-Kohlman V, Casaburi R, Davenport PW, Gandevia SC, et al. Pathophysiology of dyspnea in chronic obstructive pulmonary disease: a roundtable. Proc Am Thorac Soc 2007;4:145-68.
9. Leidy NK, Murray LT, Monz BU, et al. Measuring respiratory symptoms of COPD: performance of the EXACT- Respiratory Symptoms Tool (E-RS) in three clinical trials. Respir Res. 2014;15(1):124.
10. Gondos, T., Szabó, V., Sárkány, Á. et al. Estimation of the severity of breathlessness in the emergency department: a dyspnea score. BMC Emerg Med 17, 13 (2016). https://doi.org/10.1186/s12873-017-0125-6
11. Banzett RB, Moosavi SH. Measuring dyspnoea: new multidimensional instruments to match our 21st century understanding. Eur Respir J. 2017;49(3):1602473.
12. Sandberg J, Sundh J, Anderberg P, et al. Comparing recalled versus experienced symptoms of breathlessness ratings: An ecological assessment study using mobile phone technology. Respirology. 2022;27(10):874-881.
13. Mahler DA. Mechanisms and measurement of dyspnea in chronic obstructive pulmonary disease. Proc Am Thorac Soc. 2006;3(3):234-238.
14. Oga T, Nishimura K, Tsukino M, Hajiro T, Mishima M. Dyspnoea with activities of daily living versus peak dyspnoea during exercise in male patients with COPD. Respir Med. 2006;100(6):965-971.
15. Elasy TA, Gaddy G. Measuring subjective outcomes: rethinking reliability and validity. J Gen Intern Med. 1998;13(11):757-761.
16. Rennard S, Decramer M, Calverley PM, et al. Impact of COPD in North America and Europe in 2000: subjects' perspective of Confronting COPD International Survey. Eur Respir J. 2002;20(4):799-805.
17. Celli B, Blasi F, Gaga M, et al. Perception of symptoms and quality of life - comparison of patients' and physicians' views in the COPD MIRROR study. Int J Chron Obstruct Pulmon Dis. 2017;12:2189-2196.
18. Fletcher CM. The clinical diagnosis of pulmonary emphysema; an experimental study. Proc R Soc Med. 1952;45(9):577-584.
19. Bestall JC, Paul EA, Garrod R, Garnham R, Jones PW, Wedzicha JA. Usefulness of the Medical Research Council (MRC) dyspnoea scale as a measure of disability in patients with chronic obstructive pulmonary disease. Thorax. 1999;54(7):581-586.
20. Ong KC, Lu SJ, Soh CS. Does the multidimensional grading system (BODE) correspond to differences in health status of patients with COPD?. Int J Chron Obstruct Pulmon Dis. 2006;1(1):91-96.
21. Celli BR, Cote CG, Marin JM, et al. The body-mass index, airflow obstruction, dyspnea, and exercise capacity index in chronic obstructive pulmonary disease. N Engl J Med. 2004;350(10):1005-1012.
22. Ong KC, Earnest A, Lu SJ. A multidimensional grading system (BODE index) as predictor of hospitalization for COPD. Chest. 2005;128(6):3810-3816. doi:10.1378/chest.128.6.3810
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24. Jones PW, Adamek L, Nadeau G, Banik N. Comparisons of health status scores with MRC grades in COPD: implications for the GOLD 2011 classification. Eur Respir J. 2013;42(3):647-654.
25. Svedsater H, Roberts J, Patel C, Macey J, Hilton E, Bradshaw L. Life Impact and Treatment Preferences of Individuals with Asthma and Chronic Obstructive Pulmonary Disease: Results from Qualitative Interviews and Focus Groups. Adv Ther. 2017;34(6):1466-1481.
26. Munari AB, Gulart AA, Dos Santos K, Venâncio RS, Karloh M, Mayer AF. Modified Medical Research Council Dyspnea Scale in GOLD Classification Better Reflects Physical Activities of Daily Living. Respir Care. 2018;63(1):77-85.
27. Singh D, Agusti A, Anzueto A, et al. Global Strategy for the Diagnosis, Management, and Prevention of Chronic Obstructive Lung Disease: the GOLD science committee report 2019. Eur Respir J. 2019;53(5):1900164.
28. Zeng Y, Jiang F, Chen Y, Chen P, Cai S. Exercise assessments and trainings of pulmonary rehabilitation in COPD: a literature review. Int J Chron Obstruct Pulmon Dis. 2018;13:2013-2023.
29. Perez T, Burgel PR, Paillasseur JL, et al. Modified Medical Research Council scale vs Baseline Dyspnea Index to evaluate dyspnea in chronic obstructive pulmonary disease. Int J Chron Obstruct Pulmon Dis. 2015;10:1663-1672.
30. Mahler DA, Sethi S. Enhanced Drug and Device Development by Targeting "Relief of Dyspnea". Chest. 2020;158(2):464-466.
31. Ambrosino N, Scano G. Measurement of dyspnoea. Breathe 2004;1(2):101-107.
32. Ong KC, Wang YT. Factors associated with improvement in breathing capacity during exercise in patients with chronic obstructive pulmonary disease. Respirology. 2003;8(3):332-338.
33. Ong KC, Chong WF, Soh C, Earnest A. Comparison of different exercise tests in assessing outcomes of pulmonary rehabilitation. Respir Care. 2004;49(12):1498-1503.
34. Higashimoto Y, Ando M, Sano A, et al. Effect of pulmonary rehabilitation programs including lower limb endurance training on dyspnea in stable COPD: A systematic review and meta-analysis. Respir Investig. 2020;58(5):355-366.
35. Palmer T, Obst SJ, Aitken CR, et al. Fixed-intensity exercise tests to measure exertional dyspnoea in chronic heart and lung populations: a systematic review. Eur Respir Rev. 2023;32(169):230016.
36. O’Donnell DE, Milne KM, James MD, de Torres JP, Neder JA. Dyspnea in COPD: new mechanistic insights and management implications. Adv Ther 2020;37:41-60.
37. Jolley CJ, Luo YM, Steier J, Reilly C, Seymour J, Lunt A, et al. Neural respiratory drive in healthy subjects and in COPD. Eur Respir J 2009;33:289-97.
38. Jolley CJ, Luo YM, Steier J, Rafferty GF, Polkey MI, Moxham J. Neural respiratory drive and breathlessness in COPD. Eur Respir J. 2015;45(2):355-364.
39. Wu W, Guan L, Li X, et al. Correlation and compatibility between surface respiratory electromyography and transesophageal diaphragmatic electromyography measurements during treadmill exercise in stable patients with COPD. Int J Chron Obstruct Pulmon Dis. 2017;12:3273-3280.
40. L. Lin L, Guan L, Wu W, Chen R. Correlation of surface respiratory electromyography with esophageal diaphragm electromyography. Respir Physiol Neurobiol. 2019;259:45-52.
41. Breslin EH, Garoutte BC, Kohlman-Carrieri V, Celli BR. Correlations between dyspnea, diaphragm and sternomastoid recruitment during inspiratory resistance breathing in normal subjects. Chest. 1990;98(2):298-302.
42. Zhang DD, Lu G, Zhu XF, et al. Neural Respiratory Drive Measured Using Surface Electromyography of Diaphragm as a Physiological Biomarker to Predict Hospitalization of Acute Exacerbation of Chronic Obstructive Pulmonary Disease Patients. Chin Med J (Engl). 2018;131(23):2800-2807.
43. Murphy PB, Kumar A, Reilly C, et al. Neural respiratory drive as a physiological biomarker to monitor change during acute exacerbations of COPD. Thorax. 2011;66(7):602-608.
44. Suh ES, Mandal S, Harding R, et al. Neural respiratory drive predicts clinical deterioration and safe discharge in exacerbations of COPD. Thorax. 2015;70(12):1123-1130.
45. Celli BR, Fabbri LM, Aaron SD, et al. An Updated Definition and Severity Classification of Chronic Obstructive Pulmonary Disease Exacerbations: The Rome Proposal. Am J Respir Crit Care Med. 2021;204(11):1251-1258.
46. Ten Broeke CEM, Himmelreich JCL, Cals JWL, Lucassen WAM, Harskamp RE. The Roth score as a triage tool for detecting hypoxaemia in general practice: a diagnostic validation study in patients with possible COVID-19. Prim Health Care Res Dev. 2021;22:e56.
47. Easton PA, Hawes HG, Doig CJ, Johnson MW, Yokoba M, Wilde ER. Parasternal muscle activity decreases in severe COPD with salmeterol-fluticasone propionate. Chest. 2010;137(3):558-565.
48. Bellani G, Bronco A, Arrigoni Marocco S, et al. Measurement of Diaphragmatic Electrical Activity by Surface Electromyography in Intubated Subjects and Its Relationship With Inspiratory Effort. Respir Care. 2018;63(11):1341-1349.
49. Graßhoff J, Petersen E, Farquharson F, et al. Surface EMG-based quantification of inspiratory effort: a quantitative comparison with Pes. Crit Care. 2021;25(1):441.
50. Crimi C, Murphy P, Patout M, Sayas J, Winck JC. Lessons from COVID-19 in the management of acute respiratory failure. Breathe (Sheff). 2023;19(1):230035.
51. 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.
52. Cavalcanti JD, Fregonezi GAF, Sarmento AJ, et al. Electrical activity and fatigue of respiratory and locomotor muscles in obstructive respiratory diseases during field walking test. PLoS One. 2022;17(4):e0266365.
53. Luiso D, Villanueva JA, Belarte-Tornero LC, et al. Surface respiratory electromyography and dyspnea in acute heart failure patients. PLoS One. 2020;15(4):e0232225.
54. Gao S., Gong J, Chen B, Zhang B, Luo F, Yerabakan MO, Pan Y, Hu B. Use of Advanced Materials and Artificial Intelligence in Electromyography Signal Detection and Interpretation. Advanced Intelligent Systems 2022; 4(10): 2200063.
55. van Leuteren RW, Hutten GJ, de Waal CG, Dixon P, van Kaam AH, de Jongh FH. Processing transcutaneous electromyography measurements of respiratory muscles, a review of analysis techniques. J Electromyogr Kinesiol. 2019;48:176-186.
56. Lozano-García M, Estrada-Petrocelli L, Torres A, Rafferty GF, Moxham J, Jolley CJ, Jané R. Noninvasive Assessment of Neuromechanical Coupling and Mechanical Efficiency of Parasternal Intercostal Muscle during Inspiratory Threshold Loading. Sensors. 2021; 21(5):1781.
57. Gu X, Ren S, Shi Y, et al. Evaluation of Correlation Between Surface Diaphragm Electromyography and Airflow Using Fixed Sample Entropy in Healthy Subjects. IEEE Trans Neural Syst Rehabil Eng. 2022;30:238-250.
58. Rafols-de-Urquia M, Estrada L, Estevez-Piorno J, Sarlabous L, Jane R, Torres A. Evaluation of a Wearable Device to Determine Cardiorespiratory Parameters From Surface Diaphragm Electromyography. IEEE J Biomed Health Inform. 2019;23(5):1964-1971.
59. Jonkman AH, Warnaar RSP, Baccinelli W, et al. Analysis and applications of respiratory surface EMG: report of a round table meeting. Crit Care. 2024;28(1):2.
60. Jolley CJ, Moxham J. A physiological model of patient-reported breathlessness during daily activities in COPD. Eur Respir Rev 2009;18(112):66-79.
2. Dyspnea. Mechanisms, assessment, and management: a consensus statement. American Thoracic Society. Am J Respir Crit Care Med. 1999;159(1):321-340.
3. Parshall MB, Schwartzstein RM, Adams L, et al. An official American Thoracic Society statement: update on the mechanisms, assessment, and management of dyspnea. Am J Respir Crit Care Med. 2012;185(4):435-452.
4. Laviolette L, Laveneziana P; ERS Research Seminar Faculty. Dyspnoea: a multidimensional and multidisciplinary approach. Eur Respir J. 2014;43(6):1750-1762.
5. O'Donnell DE, Milne KM, James MD, de Torres JP, Neder JA. Dyspnea in COPD: New Mechanistic Insights and Management Implications. Adv Ther. 2020;37(1):41-60.
6. Hanania NA, O'Donnell DE. Activity-related dyspnea in chronic obstructive pulmonary disease: physical and psychological consequences, unmet needs, and future directions. Int J Chron Obstruct Pulmon Dis. 2019;14:1127-1138.
7. Ong KC. Evaluating dyspnoea in chronic obstructive pulmonary disease. Precision and Future Medicine 2021;5(2):62-68.
8. O’Donnell DE, Banzett RB, Carrieri-Kohlman V, Casaburi R, Davenport PW, Gandevia SC, et al. Pathophysiology of dyspnea in chronic obstructive pulmonary disease: a roundtable. Proc Am Thorac Soc 2007;4:145-68.
9. Leidy NK, Murray LT, Monz BU, et al. Measuring respiratory symptoms of COPD: performance of the EXACT- Respiratory Symptoms Tool (E-RS) in three clinical trials. Respir Res. 2014;15(1):124.
10. Gondos, T., Szabó, V., Sárkány, Á. et al. Estimation of the severity of breathlessness in the emergency department: a dyspnea score. BMC Emerg Med 17, 13 (2016). https://doi.org/10.1186/s12873-017-0125-6
11. Banzett RB, Moosavi SH. Measuring dyspnoea: new multidimensional instruments to match our 21st century understanding. Eur Respir J. 2017;49(3):1602473.
12. Sandberg J, Sundh J, Anderberg P, et al. Comparing recalled versus experienced symptoms of breathlessness ratings: An ecological assessment study using mobile phone technology. Respirology. 2022;27(10):874-881.
13. Mahler DA. Mechanisms and measurement of dyspnea in chronic obstructive pulmonary disease. Proc Am Thorac Soc. 2006;3(3):234-238.
14. Oga T, Nishimura K, Tsukino M, Hajiro T, Mishima M. Dyspnoea with activities of daily living versus peak dyspnoea during exercise in male patients with COPD. Respir Med. 2006;100(6):965-971.
15. Elasy TA, Gaddy G. Measuring subjective outcomes: rethinking reliability and validity. J Gen Intern Med. 1998;13(11):757-761.
16. Rennard S, Decramer M, Calverley PM, et al. Impact of COPD in North America and Europe in 2000: subjects' perspective of Confronting COPD International Survey. Eur Respir J. 2002;20(4):799-805.
17. Celli B, Blasi F, Gaga M, et al. Perception of symptoms and quality of life - comparison of patients' and physicians' views in the COPD MIRROR study. Int J Chron Obstruct Pulmon Dis. 2017;12:2189-2196.
18. Fletcher CM. The clinical diagnosis of pulmonary emphysema; an experimental study. Proc R Soc Med. 1952;45(9):577-584.
19. Bestall JC, Paul EA, Garrod R, Garnham R, Jones PW, Wedzicha JA. Usefulness of the Medical Research Council (MRC) dyspnoea scale as a measure of disability in patients with chronic obstructive pulmonary disease. Thorax. 1999;54(7):581-586.
20. Ong KC, Lu SJ, Soh CS. Does the multidimensional grading system (BODE) correspond to differences in health status of patients with COPD?. Int J Chron Obstruct Pulmon Dis. 2006;1(1):91-96.
21. Celli BR, Cote CG, Marin JM, et al. The body-mass index, airflow obstruction, dyspnea, and exercise capacity index in chronic obstructive pulmonary disease. N Engl J Med. 2004;350(10):1005-1012.
22. Ong KC, Earnest A, Lu SJ. A multidimensional grading system (BODE index) as predictor of hospitalization for COPD. Chest. 2005;128(6):3810-3816. doi:10.1378/chest.128.6.3810
23. Agustí A, Celli BR, Criner GJ, et al. Global Initiative for Chronic Obstructive Lung Disease 2023 Report: GOLD Executive Summary. Eur Respir J. 2023;61(4):2300239.
24. Jones PW, Adamek L, Nadeau G, Banik N. Comparisons of health status scores with MRC grades in COPD: implications for the GOLD 2011 classification. Eur Respir J. 2013;42(3):647-654.
25. Svedsater H, Roberts J, Patel C, Macey J, Hilton E, Bradshaw L. Life Impact and Treatment Preferences of Individuals with Asthma and Chronic Obstructive Pulmonary Disease: Results from Qualitative Interviews and Focus Groups. Adv Ther. 2017;34(6):1466-1481.
26. Munari AB, Gulart AA, Dos Santos K, Venâncio RS, Karloh M, Mayer AF. Modified Medical Research Council Dyspnea Scale in GOLD Classification Better Reflects Physical Activities of Daily Living. Respir Care. 2018;63(1):77-85.
27. Singh D, Agusti A, Anzueto A, et al. Global Strategy for the Diagnosis, Management, and Prevention of Chronic Obstructive Lung Disease: the GOLD science committee report 2019. Eur Respir J. 2019;53(5):1900164.
28. Zeng Y, Jiang F, Chen Y, Chen P, Cai S. Exercise assessments and trainings of pulmonary rehabilitation in COPD: a literature review. Int J Chron Obstruct Pulmon Dis. 2018;13:2013-2023.
29. Perez T, Burgel PR, Paillasseur JL, et al. Modified Medical Research Council scale vs Baseline Dyspnea Index to evaluate dyspnea in chronic obstructive pulmonary disease. Int J Chron Obstruct Pulmon Dis. 2015;10:1663-1672.
30. Mahler DA, Sethi S. Enhanced Drug and Device Development by Targeting "Relief of Dyspnea". Chest. 2020;158(2):464-466.
31. Ambrosino N, Scano G. Measurement of dyspnoea. Breathe 2004;1(2):101-107.
32. Ong KC, Wang YT. Factors associated with improvement in breathing capacity during exercise in patients with chronic obstructive pulmonary disease. Respirology. 2003;8(3):332-338.
33. Ong KC, Chong WF, Soh C, Earnest A. Comparison of different exercise tests in assessing outcomes of pulmonary rehabilitation. Respir Care. 2004;49(12):1498-1503.
34. Higashimoto Y, Ando M, Sano A, et al. Effect of pulmonary rehabilitation programs including lower limb endurance training on dyspnea in stable COPD: A systematic review and meta-analysis. Respir Investig. 2020;58(5):355-366.
35. Palmer T, Obst SJ, Aitken CR, et al. Fixed-intensity exercise tests to measure exertional dyspnoea in chronic heart and lung populations: a systematic review. Eur Respir Rev. 2023;32(169):230016.
36. O’Donnell DE, Milne KM, James MD, de Torres JP, Neder JA. Dyspnea in COPD: new mechanistic insights and management implications. Adv Ther 2020;37:41-60.
37. Jolley CJ, Luo YM, Steier J, Reilly C, Seymour J, Lunt A, et al. Neural respiratory drive in healthy subjects and in COPD. Eur Respir J 2009;33:289-97.
38. Jolley CJ, Luo YM, Steier J, Rafferty GF, Polkey MI, Moxham J. Neural respiratory drive and breathlessness in COPD. Eur Respir J. 2015;45(2):355-364.
39. Wu W, Guan L, Li X, et al. Correlation and compatibility between surface respiratory electromyography and transesophageal diaphragmatic electromyography measurements during treadmill exercise in stable patients with COPD. Int J Chron Obstruct Pulmon Dis. 2017;12:3273-3280.
40. L. Lin L, Guan L, Wu W, Chen R. Correlation of surface respiratory electromyography with esophageal diaphragm electromyography. Respir Physiol Neurobiol. 2019;259:45-52.
41. Breslin EH, Garoutte BC, Kohlman-Carrieri V, Celli BR. Correlations between dyspnea, diaphragm and sternomastoid recruitment during inspiratory resistance breathing in normal subjects. Chest. 1990;98(2):298-302.
42. Zhang DD, Lu G, Zhu XF, et al. Neural Respiratory Drive Measured Using Surface Electromyography of Diaphragm as a Physiological Biomarker to Predict Hospitalization of Acute Exacerbation of Chronic Obstructive Pulmonary Disease Patients. Chin Med J (Engl). 2018;131(23):2800-2807.
43. Murphy PB, Kumar A, Reilly C, et al. Neural respiratory drive as a physiological biomarker to monitor change during acute exacerbations of COPD. Thorax. 2011;66(7):602-608.
44. Suh ES, Mandal S, Harding R, et al. Neural respiratory drive predicts clinical deterioration and safe discharge in exacerbations of COPD. Thorax. 2015;70(12):1123-1130.
45. Celli BR, Fabbri LM, Aaron SD, et al. An Updated Definition and Severity Classification of Chronic Obstructive Pulmonary Disease Exacerbations: The Rome Proposal. Am J Respir Crit Care Med. 2021;204(11):1251-1258.
46. Ten Broeke CEM, Himmelreich JCL, Cals JWL, Lucassen WAM, Harskamp RE. The Roth score as a triage tool for detecting hypoxaemia in general practice: a diagnostic validation study in patients with possible COVID-19. Prim Health Care Res Dev. 2021;22:e56.
47. Easton PA, Hawes HG, Doig CJ, Johnson MW, Yokoba M, Wilde ER. Parasternal muscle activity decreases in severe COPD with salmeterol-fluticasone propionate. Chest. 2010;137(3):558-565.
48. Bellani G, Bronco A, Arrigoni Marocco S, et al. Measurement of Diaphragmatic Electrical Activity by Surface Electromyography in Intubated Subjects and Its Relationship With Inspiratory Effort. Respir Care. 2018;63(11):1341-1349.
49. Graßhoff J, Petersen E, Farquharson F, et al. Surface EMG-based quantification of inspiratory effort: a quantitative comparison with Pes. Crit Care. 2021;25(1):441.
50. Crimi C, Murphy P, Patout M, Sayas J, Winck JC. Lessons from COVID-19 in the management of acute respiratory failure. Breathe (Sheff). 2023;19(1):230035.
51. 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.
52. Cavalcanti JD, Fregonezi GAF, Sarmento AJ, et al. Electrical activity and fatigue of respiratory and locomotor muscles in obstructive respiratory diseases during field walking test. PLoS One. 2022;17(4):e0266365.
53. Luiso D, Villanueva JA, Belarte-Tornero LC, et al. Surface respiratory electromyography and dyspnea in acute heart failure patients. PLoS One. 2020;15(4):e0232225.
54. Gao S., Gong J, Chen B, Zhang B, Luo F, Yerabakan MO, Pan Y, Hu B. Use of Advanced Materials and Artificial Intelligence in Electromyography Signal Detection and Interpretation. Advanced Intelligent Systems 2022; 4(10): 2200063.
55. van Leuteren RW, Hutten GJ, de Waal CG, Dixon P, van Kaam AH, de Jongh FH. Processing transcutaneous electromyography measurements of respiratory muscles, a review of analysis techniques. J Electromyogr Kinesiol. 2019;48:176-186.
56. Lozano-García M, Estrada-Petrocelli L, Torres A, Rafferty GF, Moxham J, Jolley CJ, Jané R. Noninvasive Assessment of Neuromechanical Coupling and Mechanical Efficiency of Parasternal Intercostal Muscle during Inspiratory Threshold Loading. Sensors. 2021; 21(5):1781.
57. Gu X, Ren S, Shi Y, et al. Evaluation of Correlation Between Surface Diaphragm Electromyography and Airflow Using Fixed Sample Entropy in Healthy Subjects. IEEE Trans Neural Syst Rehabil Eng. 2022;30:238-250.
58. Rafols-de-Urquia M, Estrada L, Estevez-Piorno J, Sarlabous L, Jane R, Torres A. Evaluation of a Wearable Device to Determine Cardiorespiratory Parameters From Surface Diaphragm Electromyography. IEEE J Biomed Health Inform. 2019;23(5):1964-1971.
59. Jonkman AH, Warnaar RSP, Baccinelli W, et al. Analysis and applications of respiratory surface EMG: report of a round table meeting. Crit Care. 2024;28(1):2.
60. Jolley CJ, Moxham J. A physiological model of patient-reported breathlessness during daily activities in COPD. Eur Respir Rev 2009;18(112):66-79.