The major limitation to exercise performance in COPD is dynamic hyperinflation
2008; American Physiological Society; Volume: 105; Issue: 2 Linguagem: Inglês
10.1152/japplphysiol.90336.2008b
ISSN8750-7587
AutoresDenis E. O’Donnell, Katherine A. Webb,
Tópico(s)Cardiovascular and exercise physiology
ResumoPOINT-COUNTERPOINTThe major limitation to exercise performance in COPD is dynamic hyperinflationDenis E. O'Donnell, and Katherine A. WebbDenis E. O'Donnell, and Katherine A. WebbPublished Online:01 Aug 2008https://doi.org/10.1152/japplphysiol.90336.2008bMoreSectionsPDF (154 KB)Download PDF ToolsExport citationAdd to favoritesGet permissionsTrack citations ShareShare onFacebookTwitterLinkedInWeChat The inability to engage in sustained physical activity is a common feature of chronic obstructive pulmonary disease (COPD) and contributes importantly to the perception of poor health status. Given the vast pathophysiological heterogeneity of this disease, the concomitant effects of aging on physical performance, and the existence in many serious comorbidities, the mechanisms of exercise intolerance are necessarily complex and multifactorial. Recognized contributory factors to exercise limitation include critical dynamic physiological impairment of the ventilatory, cardiovascular, metabolic, and locomotor muscle systems in highly variable combinations. In practice, intolerable exertional symptoms limit exercise performance even before physiological maxima are reached: in more advanced COPD, perceived respiratory difficulty (dyspnea) is usually the proximate limiting symptom (10, 12).Expiratory flow-limitation (EFL) and lung hyperinflation that are only partially reversible to bronchodilator therapy are pathophysiological hallmarks of COPD. Static lung hyperinflation refers to the resetting of the respiratory system's relaxation volume to a higher level as a result of the increased static lung compliance of emphysema. When EFL is present during resting spontaneous breathing, end-expiratory lung volume (EELV) is also dynamically determined and varies with the mechanical time constant for emptying (the product of resistance and compliance) of the respiratory system, the inspired tidal volume, and the expiratory time available.Breathing at higher lung volumes increases airway conductance at rest in flow-limited patients with COPD. Moreover, the insidious development of thoracic hyperinflation over decades is associated with several adaptations that remarkably preserve the force-generating capacity of the diaphragm (27).The existence of significant lung hyperinflation at rest means that the patients' ability to increase ventilation when the situation demands it (e.g., exercise) is seriously curtailed. During exercise, the combination of increased ventilatory requirements (mainly secondary to increased ventilation/perfusion mismatching) and abnormal dynamic ventilatory mechanics stresses the already diminished cardiopulmonary reserves of patients with COPD. Reduced peak oxygen uptake has been found to correlate well with the low resting inspiratory capacity (IC; reflecting increased EELV) in patients with demonstrable resting EFL, confirming that mechanical factors contribute importantly to exercise limitation (5, 17, 25).The temporary and variable increase in EELV above the “static” value that occurs when ventilation is acutely increased is termed dynamic pulmonary hyperinflation (DH; Fig. 2). DH occurs during exercise in flow-limited patients despite active recruitment of expiratory muscles (12, 15). Pneumotachygraphic IC measurements are reliable (16, 31) and changes accurately reflect changes in EELV during exercise as total lung capacity (TLC) remains unaltered (28, 31). Significant DH (by ∼0.5 l) has recently been documented in symptomatic patients with early COPD (GOLD stage I) and was associated with reduced peak oxygen uptake (19). In recent studies in 430 patients with moderate to severe COPD (FEV1.0 40% predicted), IC at peak exercise was reduced by an average of 20% of the already reduced resting value (10, 14). Fifteen percent of COPD patients did not significantly decrease IC during incremental or constant work rate cycle exercise. These included: 1) patients with milder COPD (the minority) who increased or maintained IC during exercise and 2) patients with severe resting lung hyperinflation who could not decrease IC any further.In a recent mechanical study, DH early in exercise (by attenuating EFL) permitted acute increases in submaximal ventilation (to ∼30 l/min) and concomitant inspiratory effort (to ∼40% maximum) without provoking significant breathing discomfort (Borg ratings ∼2 “slight”; Ref. 15).However, as end-inspiratory lung volume expanded to reach a minimal inspiratory reserve volume (IRV) of ∼0.4 liters below TLC, the inspiratory muscles become functionally weakened and burdened with significant increases in elastic and inspiratory threshold loading (i.e., auto-PEEP effect). When the minimal IRV was reached, dyspnea subsequently escalated to intolerable levels at a point where their inspiratory and expiratory muscles used ∼50 and 10% of their maximal possible force generating capacity, respectively.DH results in restrictive mechanical constraints (see Fig. 2), which in the extreme can lead to alveolar hypoventilation during exercise (13). The smaller the resting IC (and IRV), the lower the ventilation (and work rate) at which a VT plateau is discernible. The consequent tachypnea will result in an increased velocity of shortening of the inspiratory muscles (with further functional weakness; Ref. 24) as well as sharp decreases in dynamic lung compliance. DH, particularly if it is accompanied by excessive expiratory muscle activity, also has the potential to adversely effect cardiocirculatory function, and thus ventilatory/locomotor muscle interactions, during exercise in COPD (1, 23). When impairment of cardiac output (and oxygen transport) is coupled with severely compromised ventilatory muscle function, the development of inspiratory muscle fatigue is possible. However, objective diaphragmatic fatigue has not been consistently demonstrated at the limits of tolerance in COPD (9, 21).In health, the ratio of tidal inspiratory effort (esophageal pressure relative to the maximum) to VT displacement—the effort-displacement ratio—remains essentially unaltered throughout much of symptom-limited cycle exercise, indicating the optimal position of operating volume on the pressure-volume relationship of the respiratory system (12) (see Fig. 2). By contrast, this ratio increases approximately twofold during exercise in COPD, reflecting “high-end mechanics” and consequent neuromechanical uncoupling of the respiratory system as a result of DH (12, 15). In essence, a situation arises during activity in the patient with COPD where, despite expending the most vigorous inspiratory efforts, very little air enters the lungs with each breath.Several studies have shown that dyspnea intensity is strongly correlated with indexes of mechanical restriction (reduced dynamic IC and IRV, increased VT/IC ratio) and with increased effort-displacement ratios that rise precipitously when VT expands to reach the minimal IRV (12,15). We postulate that in COPD, a mismatch between central neural drive (sensed via increased central corollary discharge; Ref. 3) and the abnormal “restricted” mechanical response (conveyed by afferent inputs from abundant respiratory mechanosensors) is fundamental to the origin of dyspnea or its major qualitative dimensions (11).The contention that lung hyperinflation contributes importantly to dyspnea and exercise intolerance in COPD has been bolstered by a number of intervention studies (2, 6–8, 10, 14–16, 18, 20, 22). All classes of bronchodilators act by relaxing airway smooth muscle tone, thereby decreasing the mechanical time constants for emptying in heterogeneously distributed alveolar units. Sustained increases in the resting IC (reflecting lung deflation) in the order of 0.3 liters or ∼10–15% predicted (or 15–17% of baseline value) appear to be clinically meaningful (2, 10, 15, 16, 20). Greater IC recruitment (e.g., 0.5 liters) is possible with combined long-acting bronchodilators (31).In moderate-to severe COPD patients, improvement in the resting and dynamic IC has been shown to correlate well with: 1) improved peak symptom-limited oxygen uptake and constant work endurance time (4, 14–16, 20), 2) increased peak VT (14, 15, 20), and 3) reduced dyspnea intensity (4, 14, 15, 20). In all of these studies, increased resting IC was linked to a deeper slower breathing pattern during exercise. Moreover, bronchodilator therapy was associated with reduced resistive and elastic/threshold loading of the inspiratory muscles, which resulted in a reduced oxygen cost of breathing compared with placebo (15). Lung volume deflation was also linked to increased ventilatory muscle strength and reduced fractional effort requirements for a given VT displacement (15).Decreased dyspnea intensity ratings correlate with improved effort-displacement ratios and increased VT during exercise (8, 15). Pharmacological lung volume reduction is associated with minor improvements in cardiac performance during exercise (26, 29). In carefully selected patients, lung volume reduction surgery (LVRS) and bullectomy has similarly been shown to improve operating lung volumes, effort-displacement ratios, exertional dyspnea, and exercise performance (8, 18). Surprisingly, LVRS was not associated with positive short- or long-term effects on cardiac hemodynamics, at least at rest (4). Finally, interventions such as hyperoxia (alone or in combination; Refs. 6, 20) and exercise training (22) have been shown to reduce the rate of DH during exercise (mainly by reducing breathing frequency), thereby contributing to improved dyspnea and exercise endurance.In conclusion, although activity limitation in COPD is multifactorial, there is now compelling evidence that acute derangements in dynamic ventilatory mechanics contribute importantly. Therapies aimed at partially reversing pulmonary hyperinflation represent the first step in improving dyspnea and exercise capacity, thus facilitating rehabilitation in symptomatic patients with COPD. FIg. 2.Dyspnea intensity, operating lung volumes, breathing pattern, and the effort displacement ratio are shown during incremental exercise in patients with COPD and in age-matched healthy individuals (Normal). Dyspnea intensity is greater and breathing pattern is relatively rapid and shallow in COPD compared with health. In COPD, tidal volume (VT) takes up a larger proportion of the reduced inspiratory capacity (IC) at any given ventilation—mechanical constraints on tidel volume expansion are additionally compounded because of dynamic hyperinflation during exercise. In COPD compared with health, tidal insporatory pressure swings expressed as a fraction of their maximal force-generating capacity (Pes/PImax) are greater and the VT response expressed as a fraction of the predicted vital capacity (VC) is reduced, i.e., the effort-displacement ratio is increased. TLC, total lung capacity; F, breathing frequency. Values are shown as means of data from Ref. 12.Download figureDownload PowerPointREFERENCES1 Aliverti A, Dellacà RL, Lotti P, Bertini S, Duranti R, Scano G, Heyman J, Lo Mauro A, Pedotti A, Macklem PT. Influence of expiratory flow-limitation during exercise on systemic oxygen delivery in humans. Eur J Appl Physiol 95: 229–242, 2005.Crossref | ISI | Google Scholar2 Belman MJ, Botnick WC, Shin JW. Inhaled bronchodilators reduce dynamic hyperinflation during exercise in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 153: 967–975, 1996.Crossref | ISI | Google Scholar3 Chen Z, Eldridge FL, Wagner PG. Respiratory-associated thalamic activity is related to level of respiratory drive. Respir Physiol 90: 99–113, 1992.Crossref | Google Scholar4 Criner GJ, Scharf SM, Falk JA, Gaughan JP, Sternberg AL, Patel NB, Fessler HE, Minai OA, Fishman AP, for the National Emphysema Treatment Trial Research Group. Effect of lung volume reduction surgery on resting pulmonary hemodynamics in severe emphysema. Am J Respir Crit Care Med 176: 253–260, 2007.Crossref | ISI | Google Scholar5 Diaz O, Villafranca C, Ghezzo H, Borzone G, Leiva A, Milic-Emili J, Lisboa C. Role of inspiratory capacity on exercise tolerance in COPD patients with and without tidal expiratory flow limitation at rest. Eur Respir J 16: 269–275, 2000.Crossref | ISI | Google Scholar6 Eves ND, Petersen SR, Haykowsky MJ, Wong EY, Jones RL. Helium-hyperoxia, exercise, and respiratory mechanics in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 174: 763–771, 2006.Crossref | PubMed | ISI | Google Scholar7 Hopkinson NS, Toma TP, Hansell DM, Goldstraw P, Moxham J, Geddes DM, Polkey MI. Effect of bronchoscopic lung volume reduction on dynamic hyperinflation and exercise in emphysema. Am J Respir Crit Care Med 171: 453–460, 2005.Crossref | ISI | Google Scholar8 Laghi F, Jurban A, Topeli A, Fahey PJ, Garrity E Jr, Archids JM, DePinto DJ, Edwards LC, Tobin MJ. Effect of lung volume reduction surgery on neuromechanical coupling of the diaphragm. Am J Respir Crit Care Med 157: 475–483, 1998.Crossref | ISI | Google Scholar9 Mador MJ, Kufel TJ, Pineda LA, Sharma GK. Diaphragmatic fatigue and high-intensity exercise in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 161: 118–123, 2000.Crossref | PubMed | ISI | Google Scholar10 Maltais F, Hamilton A, Marciniuk D, Hernandez P, Sciurba FC, Richter K, Kesten S, O'Donnell D. Improvements in symptom-limited exercise performance over 8 h with once-daily tiotropium in patients with COPD. Chest 128: 1168–1178, 2005.Crossref | PubMed | ISI | Google Scholar11 O'Donnell DE, Banzett RB, Carrieri-Kohlman V, Casaburi R, Davenport PW, Gandevia SC, Gelb AF, Mahler DA, Webb KA. Pathophysiology of dyspnea in chronic obstructive pulmonary disease: a roundtable. Proc Am Thorac Soc 4: 145–168, 2007.Crossref | Google Scholar12 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 155: 109–115, 1997.Crossref | PubMed | ISI | Google Scholar13 O'Donnell DE, D'Arsigny C, Fitzpatrick M, Webb KA. Exercise hypercapnia in advanced chronic obstructive pulmonary disease: the role of lung hyperinflation. Am J Respir Crit Care Med 166: 663–668, 2002.Crossref | ISI | Google Scholar14 O'Donnell D, Flüge T, Gerken F, Hamilton A, Webb K, Aguilaniu B, Make B, Magnussen H. Effects of tiotropium on lung hyperinflation, dyspnoea and exercise tolerance in COPD. Eur Respir J 23: 832–840, 2004.Crossref | ISI | Google Scholar15 O'Donnell DE, Hamilton AL, Webb KA. Sensory-mechanical relationships during high-intensity, constant-work-rate exercise in COPD. J Appl Physiol 101: 1025–1035, 2006.Link | ISI | Google Scholar16 O'Donnell DE, Lam M, Webb KA. Measurement of symptoms, lung hyperinflation and endurance during exercise in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 158: 1557–1565, 1998.Crossref | PubMed | ISI | Google Scholar17 O'Donnell DE, Revill S, Webb KA. Dynamic hyperinflation and exercise intolerance in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 164: 770–777, 2001.Crossref | PubMed | ISI | Google Scholar18 O'Donnell DE, Webb KA, Bertley JC, Chau LKL, Conlan AA. Mechanisms of relief of exertional breathlessness following unilateral bullectomy and lung volume reduction surgery in emphysema. Chest 110: 18–27, 1996.Crossref | ISI | Google Scholar19 Ofir D, Laveneziana P, Webb KA, Lam YM, O'Donnell DE. Mechanisms of dyspnea during cycle exercise in symptomatic patients with GOLD stage I chronic obstructive pulmonary disease. Am J Respir Crit Care Med 177: 622–629, 2008.Crossref | PubMed | ISI | Google Scholar20 Peters MM, Webb KA, O'Donnell DE. Combined physiological effects of bronchodilators and hyperoxia on exertional dyspnoea in normoxic COPD. Thorax 61: 559–567, 2006.Crossref | ISI | Google Scholar21 Polkey MI, Kyroussis D, Keilty SE, Hamnegard CH, Mills GH, Green M, Moxham J. Exhaustive treadmill exercise does not reduce twitch transdiaphragmatic pressure in patients with COPD. Am J Respir Crit Care Med 152: 959–964, 1995.Crossref | PubMed | ISI | Google Scholar22 Porszasz J, Emtner M, Goto S, Somfay A, Whipp BJ, Casaburi R. Exercise training decreases ventilatory requirements and exercise-induced hyperinflation at submaximal intensities in patients with COPD. Chest 128: 2024–2034, 2005.Google Scholar23 Potter WA, Olafsson S, Hyatt RE. Ventilatory mechanics and expiratory flow limitation during exercise in patients with obstructive lung disease. J Clin Invest 50: 910–919, 1971.Crossref | PubMed | ISI | Google Scholar24 Pride NB, Macklem PT. Lung mechanics in disease. In: Handbook of Physiology. The Respiratory System. Bethesda, MD: Am Physiol Soc, 1986, sect. 3, vol. III, pt. 2, p. 659–692.Google Scholar25 Puente-Maestu L, Garcia de Pedro J, Martinez-Abad Y, Ruiz de Ona JM, Llorente D, Cubillo JM. Dyspnea, ventilatory pattern, and changes in dynamic hyperinflation related to the intensity of constant work rate exercise in COPD. Chest 128: 651–656, 2005.Crossref | ISI | Google Scholar26 Saito S, Miyamoto K, Nishimura M, Aida A, Saito H, Tsujino I, Kawakami Y. Effects of inhaled bronchodilators on pulmonary hemodynamics at rest and during exercise in patients with COPD. Chest 115: 376–382, 1999.Crossref | PubMed | ISI | Google Scholar27 Similowski T, Yan S, Gauthier AP, Macklem PT, Bellemare F. Contractile properties of the human diaphragm during chronic hyperinflation. N Engl J Med 325: 917–923, 1991.Crossref | PubMed | ISI | Google Scholar28 Stubbing DG, Pengelly LD, Morse JLC, Jones NL. Pulmonary mechanics during exercise in subjects with chronic airflow obstruction. J Appl Physiol 49: 511–515, 1980.Link | ISI | Google Scholar29 Travers J, Laveneziana P, Webb KA, Kesten S, O'Donnell DE. Effect of tiotropium bromide on the cardiovascular response to exercise in COPD. Respir Med 101: 2017–2024, 2007.Crossref | ISI | Google Scholar30 Van Noord JA, Aumann JL, Janssens E, Verhaert J, Smeets JJ, Mueller A, Cornellisen PJG. Effects of tiotropium with and without formoterol on airflow obstruction and resting hyperinflation in patients with COPD. Chest 129: 509–517, 2006.Crossref | ISI | Google Scholar31 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 156: 55–59, 1997.Crossref | PubMed | ISI | Google Scholar Download PDF Previous Back to Top Next FiguresReferencesRelatedInformationCited ByExpanded central role of the respiratory physiotherapists in the community setting16 November 2022 | Irish Journal of Medical Science (1971 -), Vol. 64Ergogenic value of oxygen supplementation in chronic obstructive pulmonary disease12 July 2022 | Internal and Emergency Medicine, Vol. 17, No. 5Effects of Muscle Energy Technique and Joint Manipulation on Pulmonary Functions, Mobility, Disease Exacerbations, and Health-Related Quality of Life in Chronic Obstructive Pulmonary Disease Patients: A Quasiexperimental StudyBioMed Research International, Vol. 2022Validity and reliability of a new incremental step test for people with chronic obstructive pulmonary disease6 April 2022 | BMJ Open Respiratory Research, Vol. 9, No. 1Compensatory responses to increased mechanical abnormalities in COPD during sleep16 January 2022 | European Journal of Applied Physiology, Vol. 122, No. 3Sleep-Related Breathing Complaints in Chronic Obstructive Pulmonary DiseaseSleep Medicine Clinics, Vol. 17, No. 1Tidal volume expandability affected by flow, dynamic hyperinflation, and quasi-fixed inspiratory time in patients with COPD and healthy individuals8 October 2022 | Chronic Respiratory Disease, Vol. 19The Clinical Utility of Forced Oscillation Technique (FOT) during Hospitalisation in patients with exacerbation of COPD10 December 2021 | ERJ Open ResearchImpact of chronic obstructive pulmonary disease on passive viscoelastic components of the musculoarticular system10 September 2021 | Scientific Reports, Vol. 11, No. 1Comparison between tools for measuring breathlessness: Cross‐sectional validation of the Japanese version of the Dyspnoea‐123 August 2021 | The Clinical Respiratory Journal, Vol. 15, No. 11Exercise training in COPD: muscle O 2 transport plasticity14 January 2021 | European Respiratory Journal, Vol. 58, No. 2Unravelling the mechanisms driving multimorbidity in COPD to develop holistic approaches to patient-centred care1 June 2021 | European Respiratory Review, Vol. 30, No. 160Slow chest compression acutely reduces dynamic hyperinflation in people with chronic obstructive pulmonary disease: a randomized cross-over trial8 April 2021 | Physiotherapy Theory and Practice, Vol. 41Breathing exercises in people with COPD: A realist review8 December 2020 | Journal of Advanced Nursing, Vol. 77, No. 4Assessment and treatment of airflow obstruction in patients with chronic obstructive pulmonary disorder: a guide for the clinician14 January 2021 | Expert Review of Respiratory Medicine, Vol. 15, No. 3Influence of Lung Hyperinflation on Respiratory Muscles Pressures During a Submaximal Test in Patients With COPD: A Clinical PerspectiveCurrent Respiratory Medicine Reviews, Vol. 16, No. 3Inhaled nitric oxide improves ventilatory efficiency and exercise capacity in patients with mild COPD: A randomized‐control cross‐over trial25 January 2021 | The Journal of Physiology, Vol. 166Extra-pulmonary manifestations of COPD and the role of pulmonary rehabilitation: a symptom-centered approach10 December 2020 | Expert Review of Respiratory Medicine, Vol. 15, No. 1Validation of Clinical Characteristics and Effectiveness of Pulmonary Rehabilitation in a COPD Population with Discrepancy between Exercise Tolerance and FEV16 January 2021 | Healthcare, Vol. 9, No. 1Pulmonary Rehabilitation of Chronic Obstructive Pulmonary Diseases (Review of Clinical Trials, National and International Recommendations)29 October 2020 | Bulletin of Restorative Medicine, Vol. 99, No. 5Lung Function Testing in Chronic Obstructive Pulmonary DiseaseClinics in Chest Medicine, Vol. 41, No. 3Effects of thoracic kinesio taping on pulmonary functions, respiratory muscle strength and functional capacity in patients with chronic obstructive pulmonary disease: A randomized controlled trialEXPLORE, Vol. 16, No. 5Greater exercise tolerance in COPD during acute interval, compared to equivalent constant‐load, cycle exercise: physiological mechanisms16 June 2020 | The Journal of Physiology, Vol. 598, No. 17The supine position improves but does not normalize the blunted pulmonary capillary blood volume response to exercise in mild COPDBryan A. Ross, Andrew R. Brotto, Desi P. Fuhr, Devin B. Phillips, Sean van Diepen, Tracey L. Bryan, and Michael K. Stickland13 April 2020 | Journal of Applied Physiology, Vol. 128, No. 4Combining Dynamic Hyperinflation with Dead Space Volume during Maximal Exercise in Patients with Chronic Obstructive Pulmonary Disease15 April 2020 | Journal of Clinical Medicine, Vol. 9, No. 4Determinants of the diminished exercise capacity in patients with chronic obstructive pulmonary disease: looking beyond the lungs19 January 2020 | The Journal of Physiology, Vol. 598, No. 3Pulmonary Rehabilitation in Chronic Obstructive Pulmonary Disease15 January 2020Muscle energy technique for chronic obstructive pulmonary disease: a systematic review20 August 2019 | Chiropractic & Manual Therapies, Vol. 27, No. 1The effect of carotid chemoreceptor inhibition on exercise tolerance in chronic obstructive pulmonary disease: A randomized-controlled crossover trialRespiratory Medicine, Vol. 160Effects of Non-Invasive Ventilation Combined with Oxygen Supplementation on Exercise Performance in COPD Patients with Static Lung Hyperinflation and Exercise-Induced Oxygen Desaturation: A Single Blind, Randomized Cross-Over Trial18 November 2019 | Journal of Clinical Medicine, Vol. 8, No. 11Personalized exercise training in chronic lung diseases3 July 2019 | Respirology, Vol. 24, No. 9Dynamic Hyperinflation Impairs Cardiac Performance During Exercise in COPDJournal of Cardiopulmonary Rehabilitation and Prevention, Vol. 39, No. 3Effects of Bronchoscopic Lung Volume Reduction Coil Treatment on Arterial Blood GasesJournal of Bronchology & Interventional Pulmonology, Vol. 26, No. 2Dismantling airway disease with the use of new pulmonary function indices27 March 2019 | European Respiratory Review, Vol. 28, No. 151Impact of pulmonary rehabilitation on activities of daily living in patients with chronic obstructive pulmonary diseaseA. W. Vaes, J. M. L. Delbressine, R. Mesquita, Y. M. J. Goertz, D. J. A. Janssen, N. Nakken, F. M. E. Franssen, L. E. G. W. Vanfleteren, E. F. M. Wouters, and M. A. Spruit15 March 2019 | Journal of Applied Physiology, Vol. 126, No. 3Positive expiratory pressure breathing speeds recovery of postexercise dyspnea in chronic obstructive pulmonary disease24 September 2018 | Physiotherapy Research International, Vol. 24, No. 1Pulmonary capillary blood volume response to exercise is diminished in mild chronic obstructive pulmonary diseaseRespiratory Medicine, Vol. 145Long-acting bronchodilators improve exercise capacity in COPD patients: a systematic review and meta-analysis24 January 2018 | Respiratory Research, Vol. 19, No. 1Near-infrared spectroscopy using indocyanine green dye for minimally invasive measurement of respiratory and leg muscle blood flow in patients with COPDZafeiris Louvaris, Helmut Habazettl, Harrieth Wagner, Spyros Zakynthinos, Peter Wagner, and Ioannis Vogiatzis27 September 2018 | Journal of Applied Physiology, Vol. 125, No. 3Importance of bronchoscopic lung volume reduction coil therapy in potential candidates for lung transplantationBioScience Trends, Vol. 12, No. 4The Mozart study: a relation between dynamic hyperinflation and physical activity in patients with chronic obstructive pulmonary disease?12 April 2017 | Clinical Physiology and Functional Imaging, Vol. 38, No. 3Pulmonary Rehabilitation in the Elderly5 September 2017Exercise Training in Pulmonary Rehabilitation22 December 2017Effects of umeclidinium/vilanterol on exercise endurance in COPD: a randomised study5 January 2018 | ERJ Open Research, Vol. 4, No. 1Place de l’éducation thérapeutique du patient atteint de BPCO en réhabilitation respiratoireRevue de Pneumologie Clinique, Vol. 73, No. 6Reduced COPD Exacerbation Risk Correlates With Improved FEV 1Chest, Vol. 152, No. 3Cardiorespiratory Responses to Short Bouts of Resistance Training Exercises in Individuals With Chronic Obstructive Pulmonary DiseaseJournal of Cardiopulmonary Rehabilitation and Prevention, Vol. 37, No. 5Evaluation of bronchoscopic lung volume reduction coil treatment results in patients with severe emphysema2 October 2015 | The Clinical Respiratory Journal, Vol. 11, No. 5Impact of LABA/LAMA combination on exercise endurance and lung hyperinflation in COPD: A pair-wise and network meta-analysisRespiratory Medicine, Vol. 129Physiological and sensory consequences of exercise oscillatory ventilation in heart failure-COPDInternational Journal of Cardiology, Vol. 224DNA damage and repair capacity in lymphocyte of chronic obstructive pulmonary diseases patients during physical exercise with oxygen supplementation14 December 2016 | Multidisciplinary Respiratory Medicine, Vol. 11, No. 1Reproducibility of Ventilatory Parameters, Dynamic Hyperinflation, and Performance in the Glittre-ADL Test in COPD Patients10 May 2016 | COPD: Journal of Chronic Obstructive Pulmonary Disease, Vol. 13, No. 6Effects of dynamic hyperinflation on exercise capacity and quality of life in stable COPD patients2 March 2015 | The Clinical Respiratory Journal, Vol. 10, No. 5Influence of heart failure on resting lung volumes in patients with COPDJornal Brasileiro de Pneumologia, Vol. 42, No. 4Endoscopic Lung Volume Reduction Using Endobronchial Valves in Patients with Severe Emphysema and Very Low FEV18 September 2016 | Respiration, Vol. 92, No. 4Faster reduction in hyperinflation and improvement in lung ventilation inhomogeneity promoted by aclidinium compared to glycopyrronium in severe stable COPD patients. A randomized crossover studyPulmonary Pharmacology & Therapeutics, Vol. 35Muscular and functional effects of partitioning exercising muscle mass in patients with chronic obstructive pulmonary disease - a study protocol for a randomized controlled trial27 April 2015 | Trials, Vol. 16, No. 1Does Improving Exercise Capacity and Daily Activity Represent the Holistic Perspective of a New COPD Approach?4 August 2015 | COPD: Journal of Chronic Obstructive Pulmonary Disease, Vol. 12, No. 5Dynamic hyperinflation during activities of daily living in COPD patients20 April 2015 | Chronic Respiratory Disease, Vol. 12, No. 3Impact of Endoscopic Lung Volume Reduction on Right Ventricular Myocardial Function9 April 2015 | PLOS ONE, Vol. 10, No. 4The Effect of Pulmonary Hypertension on Aerobic Exercise Capacity in Lung Transplant Candidates with Advanced Emphysema7 March 2015 | Lung, Vol. 193, No. 2Effect of Endobronchial Valve Therapy on Pulmonary Perfusion and Ventilation Distribution30 March 2015 | PLOS ONE, Vol. 10, No. 3Oxygen delivery-utilization mismatch in contracting locomotor muscle in COPD: peripheral factorsWladimir M. Medeiros, Mari C. T. Fernandes, Diogo P. Azevedo, Flavia F. M. de Freitas, Beatriz C. Amorim, Luciana D. Chiavegato, Daniel M. Hirai, Denis E. O'Donnell, and J. Alberto Neder15 January 2015 | American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, Vol. 308, No. 2Volumetric and scintigraphic changes following endoscopic lung volume reduction30 October 2014 | European Respiratory Journal, Vol. 45, No. 1The effects of dynamic hyperinflation on CT emphysema measurements in patients with COPDEuropean Journal of Radiology, Vol. 83, No. 12Cerebrovascular responses to submaximal exerci
Referência(s)