The major limitation to exercise performance in COPD is lower limb muscle dysfunction
2008; American Physiological Society; Volume: 105; Issue: 2 Linguagem: Inglês
10.1152/japplphysiol.90336.2008a
ISSN8750-7587
AutoresRichard Debigaré, François Maltais,
Tópico(s)Cardiovascular and exercise physiology
ResumoPOINT-COUNTERPOINTThe major limitation to exercise performance in COPD is lower limb muscle dysfunctionRichard Debigaré, and François MaltaisRichard Debigaré, and François MaltaisPublished Online:01 Aug 2008https://doi.org/10.1152/japplphysiol.90336.2008aMoreSectionsPDF (152 KB)Download PDF ToolsExport citationAdd to favoritesGet permissionsTrack citations Exercise intolerance is ubiquitous in patients suffering from chronic obstructive pulmonary disease (COPD). Functional impairment can be evidenced by a lower walking capacity and cycling endurance compared with age-matched healthy controls (26). Reduced functional status and low level of daily physical activity predict poor quality of life (24), high health care use (7), and mortality (9) in these patients. A comprehensive understanding of the mechanisms of exercise intolerance is therefore of utmost importance to impact on these adverse outcomes and modify the evolution of the functional impairment associated with COPD.Respiratory impairment is not sufficient in itself to explain exercise intolerance in COPD. The weak correlation between FEV1 or inspiratory capacity and exercise tolerance implies that other factors must be involved (21, 14). In 1992, Killian and collaborators (15) published a landmark paper that draws attention to the impact of the lower limb muscles on exercise intolerance in COPD. They reported that leg discomfort was a frequent exercise-limiting symptom invoked by these patients after a standardized cycling protocol. This report was the foundation of the rationale used by scientists to investigate lower limb muscle dysfunction in COPD. At that time, no one could have predicted how vast this research area would develop.Although the ventilatory system is clearly dysfunctional in COPD, we will demonstrate that peripheral limitation to exercise tolerance is frequent in patients with COPD. To persuade the reader, morphological, biochemical, and clinical evidences demonstrating causal relationship between lower limb muscle dysfunction and exercise limitation will be exposed. We will focus on the tolerance to submaximal exercises, which are particularly influenced by the function and aerobic capacity of the lower limb muscles (3).Morphological and biochemical evidences of lower limb muscle dysfunction in COPD.The prevalence of lower limb muscle atrophy in COPD ranges from 21 to 45% depending on the population being investigated and its operational definition (23, 27). Unexpectedly, muscle atrophy can even be present in patients with normal body weight (27). Given that muscle strength is mostly determined by muscle mass, muscle weakness is therefore highly prevalent in COPD (4, 11). Patients with COPD also have a poor resistance to isolated leg exercises and increased susceptibility to muscle fatigue (16), two correlates of impaired exercise capacity (1). In parallel, altered muscle energy metabolism as assessed by 31phosphorus magnetic resonance spectroscopy (30) has also been correlated to reduced exercise capacity in patients with COPD (30).Muscle atrophy and impaired energy production are accountable for muscle weakness and increased susceptibility to fatigue, two strong determinants of exercise capacity (13). The physiological link between weakness, leg fatigue, and exercise intolerance was elegantly illustrated by Hamilton and colleagues (12). They evaluated the relationship between the perception of leg fatigue, work capacity, and muscle strength in normal individuals and patients with lung diseases, most of whom had COPD. Three interrelated observations, valid in healthy individuals and patients with lung diseases, were made 1) for a given power output, the perception of leg fatigue was greater in weaker compared with stronger individuals, 2) peak exercise capacity was reduced in weak individuals, and 3) the strength of the quadriceps was a key determinant of exercise capacity, independent of the impairment in lung function.Convincing biochemical data also support the thesis that lower limb muscle dysfunction is a major contributor to exercise intolerance in COPD. At the cellular level, several morphological and structural modifications have been observed in the quadriceps of patients with moderate to severe COPD (2). These changes substantially compromise the metabolic performance and work output of activated muscles during exercise. Specifically, the morphological changes observed include reduction in type I fiber proportion (28) as well as reduction in cross-sectional area (CSA) for type I and II fibers (10, 28) that is proportional to the reported reduction in mid-thigh cross-sectional area (4). This former observation suggests that contractile protein deficit is largely responsible for both muscle atrophy and weakness and thus contribute to impaired exercise capacity.The muscle structural and energetic changes described in COPD involve a reduction in myosin heavy chain I proportion (19) and a decrease in oxidative enzyme activities (10, 17, 18), a strong determinant of muscle endurance (1). Reduced oxidative metabolism correlates significantly with peak exercise capacity independently of lung function impairment (17). Early reliance on glycolytic activity for the energy production results in higher accumulation of inorganic phosphate (30) and premature muscle acidosis from lactate production (18), two biochemical events compromising the ability to sustain repeated muscle contractions and exercise performance. These adaptations seen in COPD are indicative of a muscle tissue that is inappropriately adapted to sustain the metabolic and mechanical requirements of submaximal exercises as seen in daily functional activities and provide a strong muscular basis to lower limb muscle dysfunction and exercise intolerance in COPD.Clinical evidences of lower limb muscle dysfunction in COPD.Exercise intolerance in COPD is the result of a complex interplay between central (ventilation, dynamic hyperinflation, dyspnea) and peripheral (muscle atrophy and weakness, fatigue) factors. Although the relative contribution of these components to exercise intolerance is difficult to sort out within a single patient, clinical models illustrating the role of the lower limb muscles are available.Undisputable evidences of peripheral limitation in exercising patients with COPD were provided by Williams and collaborators (29), who found that exercise limitation persisted in single and double lung transplant recipients years after the surgery despite complete restoration of their ventilatory capacity.Direct role of lower limb muscle dysfunction on exercise intolerance was evidenced by a study evaluating the impact of muscle fatigue on the exercise response to bronchodilation (22). In that study, the occurrence of contractile fatigue of the quadriceps after constant work rate cycling exercise prevented acute bronchodilation to translate into further improvement in exercise capacity. Patients with COPD complaining of leg fatigue as the main exercise-limiting symptom are also less likely to improve exercise tolerance following bronchodilation compared with those stopping because of dyspnea (8). These studies, together with the observation described above in lung transplantation, nicely illustrate how proximal peripheral limitation to exercise prevents interventions aimed at improving lung function to translate into better functional status.Pulmonary rehabilitation exemplifies how an intervention aimed at improving muscle function has a direct and significant positive impact on exercise tolerance. The consistent improvement in exercise tolerance reported with rehabilitation cannot be attributed to changes in respiratory function but rather to its global effects on lower limb muscle function characterized by improved strength, lesser susceptibility to fatigue, and better aerobic capacity (20). To some extent, these muscular physiological benefits also contribute to the reduction in ventilatory requirements, dynamic hyperinflation, and dyspnea often seen after exercise training (5, 6). In fact, better lower limb muscle function represents the physiological foundation of exercise training in COPD (25).Conclusion.Lower limb muscles in COPD are atrophied, weak, fatigable, and metabolically inefficient. These unfavorable muscle characteristics concur to limit exercise capacity, a most debilitating feature in COPD. Taken as a whole, clinical observation and research work performed in several laboratories support the notion that lower limb muscle dysfunction is largely responsible for exercise limitation in COPD. Denying this obvious concept and omitting this relevant component of the disease will disservice our patients since lower limb muscle dysfunction can be, in contrast to lung impairment, amenable to therapy by rehabilitative strategies.GRANTSF. Maltais and R. Debigaré are research scholars of the Fonds de la Recherche en Santé du Québec. This work was supported by CIHR Grant No. MOP-84091.REFERENCES1 Allaire J, Maltais F, Doyon JF, Noel M, Leblanc P, Carrier G, Simard C, Jobin J. Peripheral muscle endurance and the oxidative profile of the quadriceps in patients with COPD. Thorax 59: 673–678, 2004.Crossref | PubMed | ISI | Google Scholar2 American Thoracic Society/European Respiratory Society. Skeletal muscle dysfunction in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 159: S1–S40, 1999.Crossref | PubMed | ISI | Google Scholar3 Astrand PO, Rodahl K. Textbook of Work Physiology. Ohio: McGraw-Hill, 1970.Google Scholar4 Bernard S, Leblanc P, Whittom F, Carrier G, Jobin J, Belleau R, Maltais F. Peripheral muscle weakness in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 158: 629–634, 1998.Crossref | PubMed | ISI | Google Scholar5 Casaburi R, Patessio A, Ioli F, Zanaboni S, Donner CF, Wasserman K. Reductions in exercise lactic acidosis and ventilation as a result of exercise training in patients with obstructive lung disease. Am Rev Respir Dis 143: 9–18, 1991.Crossref | ISI | Google Scholar6 Casaburi R, Porszasz J, Burns MR, Carithers E, Chang RSY, Cooper CB. Physiologic benefits of exercise training in rehabilitation of patients with severe chronic obstructive pulmonary disease. Am J Respir Crit Care Med 155: 1541–1551, 1997.Crossref | ISI | Google Scholar7 Decramer M, Gosselink R, Troosters T, Verschueren M, Evers G. Muscle weakness is related to utilization of health care resources in COPD patients. Eur Respir J 10: 417–423, 1997.Crossref | PubMed | ISI | Google Scholar8 Deschênes D, Pépin V, Saey D, LeBlanc P, Maltais F. Locus of symptom limitation and exercise response to bronchodilation in chronic obstructive pulmonary disease. J Cardiopulm Rehabil Prev 28: 208–214, 2008.Crossref | Google Scholar9 Garcia-Aymerich J, Lange P, Benet M, Schnohr P, Anto JM. Regular physical activity reduces hospital admission and mortality in chronic obstructive pulmonary disease: a population based cohort study. Thorax 61: 772–778, 2006.Crossref | ISI | Google Scholar10 Gosker HR, van Mameren H, van Dijk PJ, Engelen MPKJ, van der Vusse GJ, Wouters EFM, Schols AMWJ. Skeletal muscle fibre-type shifting and metabolic profile in patients with chronic obstructive pulmonary disease. Eur Respir J 19: 617–625, 2002.Crossref | PubMed | ISI | Google Scholar11 Hamilton AL, Killian KJ, Summers E, Jones NL. Muscle strength, symptom intensity and exercise capacity in patients with cardiorespiratory disorders. Am J Respir Crit Care Med 152: 2021–2031, 1995.Crossref | ISI | Google Scholar12 Hamilton AL, Killian KJ, Summers E, Jones NL. Symptom intensity and subjective limitation to exercise in patients with cardiorespiratory disorders. Chest 110: 1255–1263, 1996.Crossref | ISI | Google Scholar13 Holloszy JO, Coyle EF. Adaptations of skeletal muscle to endurance exercise and their metabolic consequences. J Appl Physiol 56: 831–838, 1984.Link | ISI | Google Scholar14 Jones NL, Killian KJ. Limitation of exercise in chronic airway obstruction. In: Chronic Obstructive Pulmonary Disease, edited by Cherniack NS. Philadelphia: Saunders, 1991, p. 196–206.Google Scholar15 Killian KJ, Leblanc P, Martin DH, Summers E, Jones NL, Campbell EJM. Exercise capacity and ventilatory, circulatory, and symptom limitation in patients with airflow limitation. Am Rev Respir Dis 146: 935–940, 1992.Crossref | PubMed | ISI | Google Scholar16 Mador MJ, Deniz O, Aggarwal A, Kufel TJ. Quadriceps fatigability after single muscle exercise in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 168: 102–108, 2003.Crossref | PubMed | ISI | Google Scholar17 Maltais F, Leblanc P, Whittom F, Simard C, Marquis K, Belanger M, Breton MJ, Jobin J. Oxidative enzyme activities of the vastus lateralis muscle and the functional status in patients with COPD. Thorax 55: 848–853, 2000.Crossref | PubMed | ISI | Google Scholar18 Maltais F, Simard AA, Simard C, Jobin J, Desgagnés P, Leblanc P. Oxidative capacity of the skeletal muscle and lactic acid kinetics during exercise in normal subjects and in patients with COPD. Am J Respir Crit Care Med 153: 288–293, 1996.Crossref | PubMed | ISI | Google Scholar19 Maltais F, Sullivan MJ, Leblanc P, Duscha BD, Schachat FH, Simard C, Blank JM, Jobin J. Altered expression of myosin heavy chain in the vastus lateralis muscle in patients with COPD. Eur Respir J 13: 850–854, 1999.Crossref | PubMed | ISI | Google Scholar20 Nici L, Donner C, Wouters E, Zuwallack R, Ambrosino N, Bourbeau J, Carone M, Celli B, Engelen M, Fahy B, Garvey C, Goldstein R, Gosselink R, Lareau S, MacIntyre N, Maltais F, Morgan M, O'Donnell D, Prefault C, Reardon J, Rochester C, Schols A, Singh S, Troosters T, and on behalf of the ATS/ERS Pulmonary Rehabilitation Writing Committee. American Thoracic Society/European Respiratory Society statement on pulmonary rehabilitation. Am J Respir Crit Care Med 173: 1390–1413, 2006.Crossref | ISI | Google Scholar21 O'Donnell DE, Lam M, Webb KA. Spirometric correlates of improvement in exercise performance after anticholinergic therapy in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 160: 542–549, 1999.Crossref | ISI | Google Scholar22 Saey D, Debigare R, Leblanc P, Mador MJ, Cote CH, Jobin J, Maltais F. Contractile leg fatigue after cycle exercise: a factor limiting exercise in patients with COPD. Am J Respir Crit Care Med 168: 425–430, 2003.Crossref | PubMed | ISI | Google Scholar23 Schols AMWJ, Soeters PB, Dingemans MC, Mostert R, Frantzen PJ, Wouters EFM. Prevalence and characteristics of nutritional depletion in patients with stable COPD eligible for pulmonary rehabilitation. Am Rev Respir Dis 147: 1151–1156, 1993.Crossref | ISI | Google Scholar24 Simpson K, Killian K, McCartney N, Stubbing DG, Jones NL. Randomised controlled trial of weightlifting exercise in patients with chronic airflow limitation. Thorax 47: 70–75, 1992.Crossref | ISI | Google Scholar25 Spruit MA, Gosselink R, Pitta F, Troosters T, Decramer M. Peripheral muscle strength training in patients with COPD. Chest 125: 1589–1590, 2004.Crossref | ISI | Google Scholar26 Troosters T, Vilaro J, Rabinovich R, Casas A, Barbera JA, Rodriguez-Roisin R, Roca J. Physiological responses to the 6-min walk test in patients with chronic obstructive pulmonary disease. Eur Respir J 20: 564–569, 2002.Crossref | ISI | Google Scholar27 Vermeeren MAP, Creutzberg EC, Schols AMWJ, Postma DS, Pieters WR, Roldaan AC, Wouters EFM. Prevalence of nutritional depletion in a large out-patient population of patients with COPD. Respir Med 100: 1349–1355, 2006.Crossref | ISI | Google Scholar28 Whittom F, Jobin J, Simard PM, Leblanc P, Simard C, Bernard S, Belleau R, Maltais F. Histochemical and morphological characteristics of the vastus lateralis muscle in COPD patients. Comparison with normal subjects and effects of exercise training. Med Sci Sports Exerc 30: 1467–1474, 1998.Crossref | PubMed | ISI | Google Scholar29 Williams TJ, Patterson GA, Mcclean PA, Zamel N, Maurer JR. Maximal exercise testing in single and double lung transplant recipients. Am Rev Respir Dis 145: 101–105, 1992.Crossref | PubMed | ISI | Google Scholar30 Wuyam B, Payen JF, Levy P, Bensaidane H, Reutenauer H, Le Bas JF, Benabid AL. Metabolism and aerobic capacity of skeletal muscle in chronic respiratory failure related to chronic obstructive pulmonary disease. Eur Respir J 5: 157–162, 1992.PubMed | ISI | Google Scholar Download PDF Previous Back to Top Next FiguresReferencesRelatedInformation Cited ByEffect of modified Total Body Recumbent Stepper training on exercise capacity and thioredoxin in COPD: a randomized clinical trial1 July 2022 | Scientific Reports, Vol. 12, No. 1Ergogenic value of oxygen supplementation in chronic obstructive pulmonary disease12 July 2022 | Internal and Emergency Medicine, Vol. 17, No. 5Validity and reliability of a new incremental step test for people with chronic obstructive pulmonary disease6 April 2022 | BMJ Open Respiratory Research, Vol. 9, No. 1Impact of chronic obstructive pulmonary disease on passive viscoelastic components of the musculoarticular system10 September 2021 | Scientific Reports, Vol. 11, No. 1Severe loss of mechanical efficiency in COVID‐19 patients8 June 2021 | Journal of Cachexia, Sarcopenia and Muscle, Vol. 12, No. 4Acute Cardiopulmonary and Muscle Oxygenation Responses to Normocapnic Hyperpnea Exercise in COPDMedicine & Science in Sports & Exercise, Vol. Publish Ahead of PrintExtra-pulmonary manifestations of COPD and the role of pulmonary rehabilitation: a symptom-centered approach10 December 2020 | Expert Review of Respiratory Medicine, Vol. 15, No. 1Assessment of knowledge, attitude, and practice towards pulmonary rehabilitation among COPD patients: A multicenter and cross-sectional survey in ChinaRespiratory Medicine, Vol. 174More Impaired Dynamic Ventilatory Muscle Oxygenation in Congestive Heart Failure than in Chronic Obstructive Pulmonary Disease7 October 2019 | Journal of Clinical Medicine, Vol. 8, No. 10Personalized exercise training in chronic lung diseases3 July 2019 | Respirology, Vol. 24, No. 9Cardiopulmonary and Muscular Interactions: Potential Implications for Exercise (In)tolerance in Symptomatic Smokers Without Chronic Obstructive Pulmonary Disease10 July 2019 | Frontiers in Physiology, Vol. 10Long-acting bronchodilators improve exercise capacity in COPD patients: a systematic review and meta-analysis24 January 2018 | Respiratory Research, Vol. 19, No. 1Combination of inspiratory and expiratory muscle training in same respiratory cycle versus different cycles in COPD patients: a randomized trial20 November 2018 | Respiratory Research, Vol. 19, No. 1Physiological Responses and Dynamic Hyperinflation Induced by Unsupported Arm Activities Involved in Multiple-Task Activities of Daily Living Test in Patients With COPDJournal of Cardiopulmonary Rehabilitation and Prevention, Vol. 38, No. 6Near-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. 3Chronic Obstructive Pulmonary Disease Education in Pulmonary Rehabilitation. An Official American Thoracic Society/Thoracic Society of Australia and New Zealand/Canadian Thoracic Society/British Thoracic Society Workshop ReportAnnals of the American Thoracic Society, Vol. 15, No. 7Exercise Training in Pulmonary Rehabilitation22 December 2017Inspiratory Muscle Training6 October 2017Prevalence and risk factors of chronic obstructive pulmonary diseases in a Hlai community in Hainan Island of China21 June 2016 | The Clinical Respiratory Journal, Vol. 12, No. 1Place de l'éducation thérapeutique du patient atteint de BPCO en réhabilitation respiratoireRevue de Pneumologie Clinique, Vol. 73, No. 6Cardiorespiratory Responses to Short Bouts of Resistance Training Exercises in Individuals With Chronic Obstructive Pulmonary DiseaseJournal of Cardiopulmonary Rehabilitation and Prevention, Vol. 37, No. 5Respiratory Muscle Strength in Patients With Chronic Obstructive Pulmonary DiseaseAnnals of Rehabilitation Medicine, Vol. 41, No. 4Skeletal muscle power and fatigue at the tolerable limit of ramp-incremental exercise in COPDDaniel T. Cannon*, Ana Claudia Coelho*, Robert Cao, Andrew Cheng, Janos Porszasz, Richard Casaburi, and Harry B. Rossiter22 December 2016 | Journal of Applied Physiology, Vol. 121, No. 6Failed upregulation of TFAM protein and mitochondrial DNA in oxidatively deficient fibers of chronic obstructive pulmonary disease locomotor muscle18 February 2016 | Skeletal Muscle, Vol. 6, No. 1Disease severity and muscular strength as predictors of arm and leg ergometry capacity in chronic respiratory disease8 June 2016 | Cardiovascular and Thoracic Open, Vol. 2Validity, Reliability, and Responsiveness of the Dutch Version of the London Chest Activity of Daily Living Scale in Patients With Severe COPDMedicine, Vol. 94, No. 49Gait mechanics in patients with chronic obstructive pulmonary disease28 February 2015 | Respiratory Research, Vol. 16, No. 1Muscular 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. 1Targeting oxidant-dependent mechanisms for the treatment of COPD and its comorbiditiesPharmacology & Therapeutics, Vol. 155Does 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. 5The Effect of Pulmonary Hypertension on Aerobic Exercise Capacity in Lung Transplant Candidates with Advanced Emphysema7 March 2015 | Lung, Vol. 193, No. 2Oxygen 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. 2Regenerative defect in vastus lateralis muscle of patients with chronic obstructive pulmonary disease25 March 2014 | Respiratory Research, Vol. 15, No. 1Preserved function and reduced angiogenesis potential of the quadriceps in patients with mild COPD17 January 2014 | Respiratory Research, Vol. 15, No. 1Association between peripheral muscle strength, exercise performance, and physical activity in daily life in patients with Chronic Obstructive Pulmonary Disease3 July 2014 | Multidisciplinary Respiratory Medicine, Vol. 9, No. 1Exercise Endurance in Chronic Obstructive Pulmonary Disease Patients at an Altitude of 2640 meters Breathing Air and Oxygen (FIO2 28% and 35%): A Randomized Crossover Trial10 October 2013 | COPD: Journal of Chronic Obstructive Pulmonary Disease, Vol. 11, No. 4Où en est-on de l'entraînement des muscles périphériques en 2014 ?Revue des Maladies Respiratoires Actualités, Vol. 6, No. 3Chronic Obstructive Pulmonary DiseaseClinics in Chest Medicine, Vol. 35, No. 1Comparison of cardiopulmonary exercise testing variables in COPD patients with and without coronary artery diseaseHeart & Lung, Vol. 43, No. 2Chronic Obstructive Pulmonary Disease10 January 2014An Official American Thoracic Society/European Respiratory Society Statement: Key Concepts and Advances in Pulmonary RehabilitationAmerican Journal of Respiratory and Critical Care Medicine, Vol. 188, No. 8Do isolated leg exercises improve dyspnea during exercise in chronic obstructive pulmonary disease?Applied Physiology, Nutrition, and Metabolism, Vol. 38, No. 9Physiologic Effects of an Ambulatory Ventilation System in Chronic Obstructive Pulmonary DiseaseAmerican Journal of Respiratory and Critical Care Medicine, Vol. 188, No. 3Limits to Ventilation (For Sure!) and Exercise (Maybe?) in Mild Chronic Obstructive Pulmonary DiseaseAmerican Journal of Respiratory and Critical Care Medicine, Vol. 187, No. 12Exercise and COPD: Therapeutic Responses, Disease-Related Outcomes, and Activity-Promotion Strategies13 March 2015 | The Physician and Sportsmedicine, Vol. 41, No. 1Prevalence of limb muscle dysfunction in patients with chronic obstructive pulmonary disease admitted to a pulmonary rehabilitation centreClinical Neurophysiology, Vol. 123, No. 11Ventilatory and Cardiocirculatory Exercise Profiles in COPDChest, Vol. 142, No. 5Heliox increases quadriceps muscle oxygen delivery during exercise in COPD patients with and without dynamic hyperinflationZafeiris Louvaris, Spyros Zakynthinos, Andrea Aliverti, Helmut Habazettl, Maroula Vasilopoulou, Vasileios Andrianopoulos, Harrieth Wagner, Peter Wagner, and Ioannis Vogiatzis1 October 2012 | Journal of Applied Physiology, Vol. 113, No. 7Influences of Spinal Anesthesia on Exercise Tolerance in Patients with Chronic Obstructive Pulmonary DiseaseAmerican Journal of Respiratory and Critical Care Medicine, Vol. 186, No. 7Factors Limiting Exercise Tolerance in Chronic Lung Diseases1 July 2012Effect of upper limb, lower limb and combined training on exercise performance, quality of life and survival in COPDEgyptian Journal of Chest Diseases and Tuberculosis, Vol. 61, No. 3Satellite Cells Senescence in Limb Muscle of Severe Patients with COPD13 June 2012 | PLoS ONE, Vol. 7, No. 6COPD Anno 2011: Emphasis on Bronch(iol)odilationJournal of Aerosol Medicine and Pulmonary Drug Delivery, Vol. 25, No. 3Comportamento da hiperinsuflação dinâmica em teste em esteira rolante em pacientes com DPOC moderada a graveJornal Brasileiro de Pneumologia, Vol. 38, No. 1La enfermedad pulmonar obstructiva crónica en el ancianoRevista Española de Geriatría y Gerontología, Vol. 47, No. 1Eccentric Cycle Exercise in Severe COPD: Feasibility of Application5 July 2011 | COPD: Journal of Chronic Obstructive Pulmonary Disease, Vol. 8, No. 4Evidence that a higher ATP cost of muscular contraction contributes to the lower mechanical efficiency associated with COPD: preliminary findingsGwenael Layec, Luke J. Haseler, Jan Hoff, and Russell S. Richardson1 May 2011 | American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, Vol. 300, No. 5Cardiopulmonary Exercise Testing in the Clinical Evaluation of Patients With Heart and Lung DiseaseCirculation, Vol. 123, No. 6Acute administration of bronchodilators on exercise tolerance in treated COPD patientsPulmonary Pharmacology & Therapeutics, Vol. 24, No. 1BPCO et inflammation : mise au point d'un groupe d'experts. Les phénotypes en lien avec l'inflammationRevue des Maladies Respiratoires, Vol. 28, No. 2Quadriceps metabolism during constant workrate cycling exercise in chronic obstructive pulmonary diseaseDidier Saey*, Bruno B. Lemire*, Philippe Gagnon, Éric Bombardier, A. Russell Tupling, Richard Debigaré, Claude H. Côté, and François Maltais1 January 2011 | Journal of Applied Physiology, Vol. 110, No. 1Associations of the Stair Climb Power Test With Muscle Strength and Functional Performance in People With Chronic Obstructive Pulmonary Disease: A Cross-Sectional StudyPhysical Therapy, Vol. 90, No. 12Intercostal Muscle Blood Flow Limitation during Exercise in Chronic Obstructive Pulmonary DiseaseAmerican Journal of Respiratory and Critical Care Medicine, Vol. 182, No. 9Physiologic limitations during daily life activities in COPD patientsRespiratory Medicine, Vol. 104, No. 8Impact of pulmonary system limitations on locomotor muscle fatigue in patients with COPDMarkus Amann, Mark S. Regan, Majd Kobitary, Marlowe W. Eldridge, Urs Boutellier, David F. Pegelow, and Jerome A. Dempsey1 July 2010 | American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, Vol. 299, No. 1Effect of enalapril on exercise cardiopulmonary performance in chronic obstructive pulmonary disease: A pilot studyPulmonary Pharmacology & Therapeutics, Vol. 23, No. 3Low Inspiratory Capacity to Total Lung Capacity Ratio Is a Risk Factor for Chronic Obstructive Pulmonary Disease ExacerbationThe American Journal of the Medical Sciences, Vol. 339, No. 5Aerobic exercise capacity in COPD patients with and without pulmonary hypertensionRespiratory Medicine, Vol. 104, No. 1Response of the respiratory muscles to rehabilitation in COPDMarc Decramer1 September 2009 | Journal of Applied Physiology, Vol. 107, No. 3Heliox Improves Oxygen Delivery and Utilization during Dynamic Exercise in Patients with Chronic Obstructive Pulmonary DiseaseAmerican Journal of Respiratory and Critical Care Medicine, Vol. 179, No. 11Mécanismes intégrés de la dyspnée et du handicap au cours de la bronchopneumopathie chronique obstructiveLa Presse Médicale, Vol. 38, No. 3The major limitation to exercise performance in COPD is inadequate energy supply to the respiratory and locomotor muscles vs. lower limb muscle dysfunction vs. dynamic hyperinflationJohn B. West1 August 2008 | Journal of Applied Physiology, Vol. 105, No. 2 More from this issue > Volume 105Issue 2August 2008Pages 751-753 Copyright & PermissionsCopyright © 2008 the American Physiological Societyhttps://doi.org/10.1152/japplphysiol.90336.2008aPubMed18678623History Published online 1 August 2008 Published in print 1 August 2008 Metrics
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