Respiratory Medicine
Volume 104, Issue 7 , Pages 925-933 , July 2010

Do obstructive and restrictive lung diseases share common underlying mechanisms of breathlessness?

  • Giorgio Scano

      Affiliations

    • Department of Internal Medicine, Section of Clinical Immunology and Respiratory Medicine, University of Florence, Italy
    • Fondazione Don C. Gnocchi, Section of Respiratory Rehabilitation, Pozzolatico, Firenze, Italy
    • Corresponding Author InformationCorresponding author at: Department of Internal Medicine, Section of Clinical Immunology and Respiratory Disease, University of Florence, Viale Morgagni 87, 50134 Careggi, Firenze, Italy. Tel.: +39 055 42 96 414; fax: +39 055 41 78 92.
  • ,
  • Giulia Innocenti-Bruni

      Affiliations

    • Fondazione Don C. Gnocchi, Section of Respiratory Rehabilitation, Pozzolatico, Firenze, Italy
  • ,
  • Loredana Stendardi

      Affiliations

    • Fondazione Don C. Gnocchi, Section of Respiratory Rehabilitation, Pozzolatico, Firenze, Italy

Received 4 September 2009 ,Accepted 22 February 2010.

References 

  1. Howell JB, Campbell EJ. Breathlessness. Blackwell Scientific Publication Oxford; 1966;
  2. Leblanc P, Bowie DM, Summers E, Jones NL, Killian KJ. Breathlessness and exercise in patients with cardiorespiratory disease. Am Rev Respir Dis. 1986;133:21–25
  3. Jones N, Killian K. Breathlessness: the campbell symposium. Hamilton: Boehringer Ingelheim; 1992;
  4. Killian KJ, Campbell EJM. Dyspnea. In:  Roussos C editors. The thorax part B. New York: Dekker; 1995;p. 1709–1747
  5. Mahler DA, Tomlinson D, Olmstead EM, Tosteson AN, O'Connor GT. Changes in dyspnea, health status, and lung function in chronic airway disease. Am J Respir Crit Care Med. 1995;151:61–65
  6. Hamilton AL, Killian KJ, Summers E, Jones NL. Symptom intensity and subjective limitation to exercise in patients with cardiorespiratory disorders. Chest. 1996;110:1255–1263
  7. Manning HL, Schwartzstein RM. Mechanism of dyspnea. In:  Mahler A editors. Dyspnea. New York: Marcel Dekker; 1998;pp. 63–95
  8. Manning HL, Schwartzstein RM. Pathophysiology of dyspnea. New Engl J Med. 1995;33:1547–1552
  9. O'Donnell DE, Ora J, Webb KA, Laveneziana P, Jensen D. Mechanism of activity-related dyspnea in pulmonary diseases. Respir Physiol Neurobiol. 2009;167:116–132
  10. Kaltraider NL, McCann WS. Respiratory response during exercise in pulmonary fibrosis and emphysema. J Clin Invest. 1937;16:23–40
  11. Stendardi L, Grazzini M, Gigliotti F, Scano G. Dyspnea and leg effort during exercise. Respir Med. 2005;99:933–942
  12. O'Donnell DE, Hamilton AL, Webb KA. Sensory-mechanical relationships during high intensity, constant-work-rate exercise in COPD. J Appl Physiol. 2006;101:1025–1035
  13. Jones NL, Rebuck AS. Tidal volume during exercise in patients with diffuse fibrosing alveolitis. Bull Europ Physiopath Resp. 1979;15:321–327
  14. Scano G, Gigliotti F, van Meerhaeghe A, De Coster A, Sergysels R. Influence of exercise and C02 on breathing pattern in patients with chronic obstructive lung disease (COLD). Eur Respir J. 1988;1:139–144
  15. Scano G, van Meerhaeghe A, Willeput R, Vachaudez JP, Sergysels R. Effect of oxygen on breathing during exercise in patients with chronic obstructive lung disease. Eur J Respir Dis. 1982;63:23–30
  16. Lanini B, Misuri G, Gigliotti F, Iandelli I, Pizzi A, Romagnoli I, et al. Perception of dyspnea in patients with neuromuscular disease. Chest. 2001;120:402–408
  17. Spinelli A, Marconi G, Gorini M, Pizzi A, Scano G. Control of breathing in patients with myasthenia gravis (MG). Am Rev Respir Dis. 1992;145:1359–1366
  18. Nanas S, Nanas J, Papazachou O, Kassiotis C, Papamichalopoulos A, Milic-Emili J, et al. Resting lung function and hemodynamic parameters as predictors of exercise capacity in patients with chronic heart failure. Chest. 2003;123:1386–1393
  19. Clark AL, Sparrow JL, Coats AJ. Muscle fatigue and dyspnoea in chronic heart failure: two sides of the same coin?. Eur Heart J. 1995;16:49–52
  20. Babb TG. Mechanical ventilator constraints in aging, lung disease, ad obesity: perspectives and brief review. Med Sci Sport. 1999;31:S12–S22
  21. Babb TG, DeLorey DS, Wyrick BL, Gardner PP. Mild obesity does not limit change in end-expiratory lung volume during cycling in young women. J Appl Physiol. 2002;92:2483–2490
  22. DeLorey DS, Wyrick BL, Babb TG. Mild to moderate obesity: implications for respiratory mechanics at rest and during exercise in young men. Int J Obes (Lond). 2005;29:1039–1047
  23. Ofir D, Laveneziana P, Webb KA, O'Donnell DE. Ventilatory and perceptual responses to cycle exercise in obese females. J Appl Physiol. 2007;102:2217–2226
  24. Romagnoli I, Laveneziana P, Clini EM, Palange P, Valli G, de Blasio F, et al. Role of hyperinflation vs. deflation on dyspnoea in severely to extremely obese subjects. Acta Physiol (Oxf). 2008;193:393–402
  25. Simon PM, Schwartzstein RM, Jw Weiss, Fencl V, Teghtsoonian M, Weimberger SE. Distinguishable types of dispnea in patients with shortness of breath. Am Rev Respir Dis. 1990;142:1009–1014
  26. Elliot MW, Adams L, Cockcroft A, MacRae KD, Murphy K, Guz A. The language of breathlessness: use of verbal descriptors by patients with cardiorespiratory disease. Am Rev Respir Dis. 1991;144:826–832
  27. Mahler DA, Harver A, Lentine T, Scott JA, Beck K, Schwartzstein RM. Descriptor of breathlessness in cardiorespiratory disease. Am J Respir Crit Care Med. 1996;154:1357–1363
  28. Simon PM, Schwartzstein RM, Weiss JW, Lahive K, Fencl V, Teghtsoonian M, et al. Distinguishable sensation of breathlessness induced in normal volunteers. Am Rev Respir Dis. 1989;140:1021–1027
  29. O'Donnell DE, Bertley JC, Chau LL, Webb KA. Qualitative aspects of exertional breathlessness in chronic airflow limitation: pathophysiologic mechanisms. Am J Respir Crit Care Med. 1997;155:109–115
  30. Scano G, Stendardi L, Grazzini M. Understanding dyspnoea by its language. Eur Respir J. 2005;25:380–385
  31. McCluskey DI. Corollary discharges: motor commands and perception. Part 2 In:  Brookhart JM,  Mountcastle VB editor. The nervous system. Handbook of physiology Section 1. vol. 2:Bethesda: American Physiological Society; 1981;p. 1415–1447
  32. Gandevia SC. Neural mechanisms underlying the sensation of breathlessness: kinaesthetic parallels between respiratory and limb muscles. Aus N Z J Med. 1988;18:83–91
  33. Chen Z, Eldridge FL, Wagner PG. Respiratory- associated thalamic activity is related to level of respiratory drive. Respir Physiol. 1992;90:99–113
  34. Killian KJ, Gandevia SC, Summers E, Campbell JM. Effect of increased lung volume on perception of breathlessness, effort, and tension. J Appl Physiol. 1984;57:686–691
  35. Demediuk BH, Manning H, Lilly J, Fencl V, Weinberger SE, Weiss JW, et al. Dissociation between dyspnea and respiratory effort. Am Rev Respir Dis. 1992;146:1222–1225
  36. Chonan T, Mulholland MB, Leitner J, Altose MD, Cherniack NS. Sensation of dyspnea during hypercapnia, exercise and voluntary hyperventilation. J Appl Physiol. 1990;68:2100–2106
  37. Schwartzstein RM, Simon PM, Weiss JW, Fencl V, Weinberger SE. Breathlessness induced by dissociation between ventilation and chemical drive. Am Rev Respir Dis. 1989;139:1231–1237
  38. Chonan T, Mulholland MB, Altose MD, Cherniack NS. Effects of changes in level and pattern of breathing on the sensation of dyspnea. J Appl Physiol. 1990;69:1290–1295
  39. Banzett RB, Lansing RW, Reid MB, Adams L, Brown R. “Air hunger” arising from increased PCO2 in mechanically ventilated quadriplegics. Respir Physiol. 1989;76:53–67
  40. Banzett RB, Lansing RW, Brown R, Topulos GP, Yager DS, Steele SM, et al. “Air hunger” arising from increased PCO2 persists after complete neuromuscular block in humans. Respir Physiol. 1990;81:1–17
  41. Manning HL, Shea SA, Schwartzstein RM, Lansing RW, Brown R, Banzett RB. Reduced tidal volume increases “air hunger” at fixed PCO2 in ventilated quadriplegics. Respir Physiol. 1992;90:19–30
  42. O'Donnell DE, Banzett RB, Carrieri-Kohlman V, Casaburi R, Davenport PW, Gandevia SC, et al. Pathophysiology of dyspnea in chronic obstructive pulmonary disease. Proc Am Thorac Soc. 2007;4:145–168
  43. Manning HL, Molinary E, Leiter JC. Effect of inspiratory flow rate on respiratory sensation and pattern of breathing. Am J Respir Crit Care Med. 1995;151:751–757
  44. Lansing RW, Im BS, Thwing JI, Legedza AT, Banzett RB. The perception of respiratory work and effort can be independent of the perception of air hunger. Am J Respir Crit Care Med. 2000;162:1690–1696
  45. Duranti R, Sanna A, Romagnoli I, Nerini M, Gigliotti F, Ambrosino N, et al. Walking modality affects respiratory muscle action and contribution to respiratory effort. Pflugers Arch. 2004;448:222–230
  46. Scano G, Filippelli M, Romagnoli I, Mancini M, Misuri G, Duranti R, et al. Hypoxic and hypercapnic breathlessness in patient with type I diabetes mellitus. Chest. 2000;117:960–967
  47. Scano G, Seghieri G, Mancini M, Filippelli M, Duranti R, Fabbri A, et al. Dyspnoea, peripheral airway involvement and respiratory muscle effort in patients with type I diabetes mellitus under good metabolic control. Cli Sci. 1999;96:499–506
  48. Coli C, Picariello M, Stendardi L, Grazzini M, Binazzi B, Duranti R, et al. Is there a link between the qualitative descriptors and the quantitative perception of dyspnea in asthma?. Chest. 2006;130:436–441
  49. La veneziana PA, Coli C, Binazzi B, Lotti P, Stendardi L, Duranti R, et al. Mechanisms of dyspnea and its language in patient with asthma. Eur Respir J. 2006;27:742–747
  50. Filippelli M, Duranti R, Gigliotti F, Bianchi R, Grazzini M, Stendardi L, et al. Overall contribution of chest wall hyperinflation to breathlessness in asthma. Chest. 2003;124:2164–2170
  51. Bianchi R, Gigliotti F, Romagnoli I, Lanini B, Castellani C, Grazzini M, et al. Chest wall kinematics and breathlessness during pursed-lip breathing in patients with COPD. Chest. 2004;125:459–465
  52. Romagnoli I, Gorini M, Gigliotti F, Bianchi R, Lanini B, Grazzini M, et al. Chest wall kinematics, respiratory muscle action and dyspnea during arm vs leg exercise in humans. Acta Physiol. 2006;188:63–73
  53. Bianchi R, Gigliotti F, Romagnoli I, Lanini B, Castellani C, Binazzi B, et al. Patterns of chest wall kinematics during volitional pursed-lip breathing in COPD at rest. Respir Med. 2007;101:1412–1418
  54. Romagnoli I, Lanini B, Binazzi B, Bianchi R, Coli C, Stendardi L, et al. Optoelectronic plethysmography has improve our knowledge of respiratory physiology and pathophysiology. Sensors. 2008;8:7951–7972
  55. El-Manshawi KJ, Killian E, Summers NL, Jones . Breathlessness during exercise with and without resistive loading. J Appl Physiol. 1986;61:896–905
  56. Ferrari K, Goti P, Misuri G, Amendola M, Rosi E, Grazzini M, et al. Chronic exertional dyspnea and respiratory muscle function in patients with chronic obstructive pulmonary disease. Lung. 1997;175:311–319
  57. Misuri G, Mancini M, Iandelli I, Duranti R, Stendardi L, Gigliotti F, et al. Respiratory muscle overloading and dyspnoea during bronchoconstriction in asthma: protective effects of fenoterol. Pulm Pharmacol Ther. 1997;10:299–304
  58. Lanini B, Gigliotti F, Coli C, Bianchi R, Pizzi A, Romagnoli I, et al. Dissociation between respiratory effort and dyspnoea in a subset of patients with stroke. Clin Sci (Lond). 2002;103:467–473
  59. Lotti P, Gigliotti F, Tesi F, Stendardi L, Grazzini M, Duranti R, et al. Respiratory muscles and dyspnea in obese non smoking subject. Lung. 2005;183:311–323
  60. Raj H, Singh WK, Anand A, Paintal AS. Sensory origin of lobeline-induced sensations: a correlative study in man and cat. J Physiol. 1995;482:235–246
  61. Zechman FR, Wiley RI. Afferent inputs to breathing: respiratory sensation. Section 3 In:  Fishman AP editors. Handbook of physiology. Part 2: The respiratory system. vol. II:Bethesda MD: American Physiological Society; 1986;p. 449–474
  62. Von Leupoldt A, Dahme B. Cortical substrates for the perception of dyspnea. Chest. 2005;128:345–354
  63. Von Leupold A, Sommer T, Kegat S, Baumann HJ, Klose H, Dahme B, et al. The unpleasantness of perceived dyspnea is processed in the anterior insula and amygdale. Am J Respir Crit Care Med. 2008;177:1026–1032
  64. O'Donnell DE, Revill SM, Webb AK. Dynamic hyperinflation and exercise intolerance in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2001;164:770–777
  65. O'Donnell DE, Webb KA. Exertional breathlessness in patients with chronic airflow limitation. The role of lung hyperinflation. Am Rev Respir Dis. 1993;148:1351–1357
  66. Gigliotti F, Coli C, Bianchi R, Romagnoli I, Lanini B, Binazzi B, et al. Exercise training improves exertional dyspnea in patients with COPD. Chest. 2003;123:1794–1802
  67. Gorini M, Misuri G, Corrado A, Duranti R, Iandelli I, De Paola E, et al. Breathing pattern and carbon dioxide retention in severe chronic obstructive pulmonary disease. Thorax. 1996;51:677–683
  68. Scano G, Ambrosino N. Pathophysiology of dyspnea. Lung. 2002;180:131–148
  69. O'Donnell DE, Hong HH, Webb KA. Respiratory sensation during chest wall restriction and dead space loading in exercising men. J Appl Physiol. 2000;88:1859–1869
  70. Harty HR, Corfield DR, Schwartzstein RM, Adams L. External thoracic restriction, respiratory sensation, and ventilation during exercise in men. J Appl Physiol. 1999;86:1142–1150
  71. O'Donnell DE, Chau LKL, Webb AK. Qualitative aspects of exertional dyspnea in patients with interstitial lung disease. J Appl Physiol. 1998;84:2000–2009
  72. Ferrari K, Goti P, Sanna A, Misuri G, Gigliotti F, Duranti R, et al. Short term effects of bracing on exercise performance in mild idiopathic thoracic scoliosis. Lung. 1997;175:299–310
  73. Romagnoli I, Gigliotti F, Galarducci A, Lanini B, Bianchi R, Cammelli D, et al. Chest wall kinematics and respiratory muscle action in ankylosing spondylitis patients. Eur Respir J. 2004;24:453–460
  74. Begin R, Bureau MA, Lupien L, Bernier JP, Lemieux B. Pathogenesis of respiratory insufficiency in myotonic dystrophy. Am Rev Respir Dis. 1982;125:312–318
  75. Misuri G, Lanini B, Gigliotti F, Iandelli I, Pizzi A, Bertolini MG, et al. Mechanism of CO2 retention in patients with neuromuscular disease. Chest. 2000;117:447–453
  76. Rochester DF. The diaphragm in COPD: better than expected, but not good enough. N Engl J Med. 1991;325:961–962
  77. Van Meerhaeghe A, Scano G, Sergysels R, Bran M, De Coster A. Respiratory drive and ventilatory pattern during exercise in interstitial lung disease. Bull Europ Physiopath Resp. 1981;17:15–26
  78. Gorini M, Spinelli A, Ginanni R, Duranti R, Gigliotti F, Arcangeli P, et al. Neural respiratory drive and neuromuscular coupling during CO2 rebreathing in patients with chronic interstitial lung disease. Chest. 1989;96:824–830
  79. Marciniuk DD, Sridhar G, Clemens RE, Zintel TA, Gallagher CG. Lung volumes and expiratory flow limitation during exercise in interstitial lung disease. J Appl Physiol. 1994;77:963–973
  80. Gibson GJ, Pride NB. Pulmonary mechanics in fibrosing alveolitis: the effect of lung shrinkage. Am Rev Respir Dis. 1997;116:637–647
  81. Guz A, Noble MIM, Eisele JH, Trenchard D., 1970. Experimental results of vagal block in cardiopulmonary disease. In: Breathing: Hering–Breuer Centenary Symposium. Porter R, (Ed), London: Churchill, p. 315.
  82. Binks AP, Moosavi SH, Banzett RB, Schwartzstein RM. “Tightness” sensation of asthma does not arise from the work of breathing. Am J Respir Crit Care Med. 2002;165:78–82
  83. Paintal AS. Sensations from J receptors. NIPS. 1995;10:238–243
  84. Winning AJ, Hamilton RD, Guz A. Ventilation and breathlessness on maximal exercise in patients with interstitial lung disease after local anaesthetic aerosol inhalation. Clin Sci (Lond). 1988;74:275–281
  85. Frank NR, Lyons HA, Siebens AA, Nealon TF. Pulmonary compliance in patients with cardiac disease. Am J Med. 1957;22:516–523
  86. Saxton GA, Rabinowitz M, Dexter L, Haynes F. The relationship of pulmonary compliance to pulmonary vascular pressures in patients with heart disease. J Clin Invest. 1956;35:611–618
  87. Milici-Emili G, Petit JM. Mechanical efficiency of breathing. J Appl Physiol. 1960;15:359–362
  88. D'Arsigny C, Webb KA, Raj S, Abdollah H, O'Donnell DE. Ventilatory constraints contribute to exercise limitation and dyspnea in stable congestive heart failure. Am J Respir Crit Care Med. 1999;159:A418
  89. Snashall PD, Chung KF. Airway obstruction and bronchial hyperresponsiveness in left ventricular failure and mitral stenosis. Am Rev Respir Dis. 1991;144:945–956
  90. Laveneziana P, O'Donnell DE, Ofir D, Agostoni P, Padeletti L, Ricciardi G, et al. Effect of biventricular pacing on ventilatory and perceptual responses to exercise in patients with stable chronic heart failure. J Appl Physiol. 2009;106:1574–1583
  91. Sullivan MJ, Higginbotham MB, Cobb FR. Increased exercise ventilation in patients with chronic heart failure: intact ventilatory control despite hemodynamic and pulmonary abnormalities. Circulation. 1988;77:552–559
  92. Ponikowski P, Francis DP, Piepoli MF, Davies LC, Chua TP, Davos CH, et al. Enhanced ventilatory response to exercise in patients with chronic heart failure and preserved exercise tolerance: marker of abnormal cardiorespiratory reflex control and predictor of poor prognosis. Circulation. 2001;103:967–972
  93. O'Donnell DE, D'Arsigny C, Raj S, Abdollah H, Webb KA. Ventilatory assistance improves exercise endurance in stable congestive heart failure. Am J Resp Crit Care Med. 1999;160:1804–1811
  94. Agostoni P, Pellegrino R, Conca C, Rodarte JR, Brusasco V. Exercise hyperpnea in chronic heart failure: relationships to lung stiffness and expiratory flow limitation. J Appl Physiol. 2002;92:1409–1416
  95. McParland C, Krishnan B, Wang Y, Gallagher CG. Inspiratory muscle weakness and dyspnea in chronic heart failure. Am Rev Respir Dis. 1992;146:467–472
  96. Hammond MD, Bauer KA, Sharp JT, Rocha RD. Respiratory muscle strength in congestive heart failure. Chest. 1990;908:1091–1094
  97. Naimark A, Cherniack RM. Compliance of the respiratory system and its components in health and obesity. 1960;15: 377–82.
  98. Sharp JT, Henry JP, Sweany SK, Meadows WR, Pietras RJ. The total work of breathing in normal and obese men. J Clin Invest. 1964;43:728–739
  99. Pelosi P, Croci M, Ravagnan I, Tredici S, Pedoto A, Lissoni A, et al. The effects of body mass on lung volumes, respiratory mechanics, and gas exchange during general anesthesia. Anesth Analg. 1998;87:654–660
  100. Yap JC, Watson RA, Gilbey S, Pride NB. Effects of posture on respiratory mechanics in obesity. J Appl Physiol. 1995;79:1199–1205
  101. Henke KG, Sharratt M, Pegelow D, Dempsey JA. Regulation of end-expiratory lung volume during exercise. J Appl Physiol. 1988;64:135–146
  102. Binazzi B, Lanini B, Bianchi R, Romagnoli I, Nerini M, Gigliotti F, et al. Breathing pattern and kinematics in normal subjects during speech, singing and loud whispering. Acta Physiol. 2006;186:233–246
  103. O'Donnell DE, Sanii R, Anthonisen NR, Younes M. Effect of dynamic airway compression on breathing pattern and respiratory sensation in severe chronic obstructive pulmonary disease. Am Rev Respir Dis. 1987;135:912–918
  104. O'Donnell DE, Sanii R, Younes M. External mechanical loading in conscious humans: role of upper airway mechanoreceptors. J Appl Physiol. 1988;65:541–548

PII: S0954-6111(10)00089-2

doi: 10.1016/j.rmed.2010.02.019

Respiratory Medicine
Volume 104, Issue 7 , Pages 925-933 , July 2010