Skeletal muscle dysfunction in patients with chronic obstructive pulmonary disease

Hussain, Sabah; Cheol, Kim; Mofarrahi, M

doi:10.2147/copd.s4480

Cited by 224Chronic Obstructive Pulmonary Disease (COPD) ResearchMuscle Physiology and DisordersNutrition and Health in Aging

Skeletal muscle dysfunction in patients with chronic obstructive pulmonary disease

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Hussain, Sabah, Cheol, Kim, Mofarrahi, M·2008·International Journal of Chronic Obstructive Pulmonary Disease

DOI 10.2147/copd.s4480PMC PMC2650609

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Abstract

Chronic obstructive pulmonary disease (COPD) is a debilitating disease characterized by inflammation-induced airflow limitation and parenchymal destruction. In addition to pulmonary manifestations, patients with COPD develop systemic problems, including skeletal muscle and other organ-specific dysfunctions, nutritional abnormalities, weight loss, and adverse psychological responses. Patients with COPD often complain of dyspnea on exertion, reduced exercise capacity, and develop a progressive decline in lung function with increasing age. These symptoms have been attributed to increases in the work of breathing and in impairments in gas exchange that result from airflow limitation and dynamic hyperinflation. However, there is mounting evidence to suggest that skeletal muscle dysfunction, independent of lung function, contributes significantly to reduced exercise capacity and poor quality of life in these patients. Limb and ventilatory skeletal muscle dysfunction in COPD patients has been attributed to a myriad of factors, including the presence of low grade systemic inflammatory processes, nutritional depletion, corticosteroid medications, chronic inactivity, age, hypoxemia, smoking, oxidative and nitrosative stresses, protein degradation and changes in vascular density. This review briefly summarizes the contribution of these factors to overall skeletal muscle dysfunction in patients with COPD, with particular attention paid to the latest advances in the field.

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Inactivity leads to muscle deconditioning, with reduced oxidative capacity, muscle fibre atrophy and fibre type shift from type 1 to type IIb fibres.
“However, inactivity leads to muscle deconditioning, with reduced oxidative capacity, muscle fibre atrophy and fibre type shift from type 1 (oxidative) to type IIb (glycolytic) fibres.”
From The Breathing, Thinking, Functioning clinical model: a proposal to facilitate evidence-based breathlessness management in chronic respiratory disease (2017) · cites this paper as [35]
The Inactivity section says physical inactivity causes deconditioning, reduced oxidative capacity, fiber atrophy, and a lower proportion of type I fibers. The Fiber type shift section reports increased type IIb fibers in patients with severe COPD, but does not establish that inactivity alone causes that specific shift; the Inactivity section cautions that inactivity does not fully explain muscle dysfunction in COPD. Page numbers were not available in our copy. (LLM, conf=0.85)
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“Similarly, 13% and 23% reductions in sniff Pdi and twitch Pdi (generated by phrenic stimulation) have been observed in elderly subjects, as compared to young subjects (Polkey et al 1997).”
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Upregulation of pro-inflammatory cytokines in the intercostal muscles of COPD patients
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Modifications of proteins by 4-hydroxy-2-nonenal in the ventilatory muscles of rats
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The apoptotic response to strenuous exercise of the gastrocnemius and solues muscle fibers in rats
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The oxidation produced by hydrogen peroxide on Ca‐ATP‐G‐actin
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Strenuous resistive breathing induces proinflammatory cytokines and stimulates the HPA axis in humans.
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Peripheral muscle composition and health status in patients with COPD
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Profiling of mRNA Expression in Quadriceps of Patients with COPD and Muscle Wasting
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Role of endothelium-derived relaxing factor in active hyperemia of the canine diaphragm
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Assessment of muscle fatigue during exercise in chronic obstructive pulmonary disease
Saey, D., Côt́e, C. H., Mador, M. J., Laviolette, L., Leblanc, P., Jobin, J., & Maltais, F. (2006) · Muscle & Nerve · doi:10.1002/mus.20541 · Cited by 43 · see citing works
Uncoupling Protein-3 Content Is Decreased in Peripheral Skeletal Muscle of Patients with COPD
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Actin Cross-Linking and Inhibition of the Actomyosin Motor
Kim, E., Bobkova, E. A., Hegyi, G., Mühlrád, A., & Reisler, E. (2001) · Biochemistry · doi:10.1021/bi0113824 · Cited by 42 · see citing works
Parasternal intercostal muscle remodeling in severe chronic obstructive pulmonary disease
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In vivo aging of rat skeletal muscle sarcoplasmic reticulum Ca-ATPase. Chemical analysis and quantitative simulation by exposure to low levels of peroxyl radicals
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Active Site Modifications of the Brain Isoform of Creatine Kinase by 4-Hydroxy-2-nonenal Correlate with Reduced Enzyme Activity: Mapping of Modified Sites by Fourier Transform-Ion Cyclotron Resonance Mass Spectrometry
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Dual morphometrical changes of the deltoid muscle in patients with COPD
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Oxidation and structural perturbation of redox-sensitive enzymes in injured skeletal muscle
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Scaling skeletal muscle function to mass in patients with moderate-to-severe COPD
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COPD Results in a Reduction in UCP3 Long mRNA and UCP3 Protein Content in Types I and IIa Skeletal Muscle Fibers
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Oxidative and nitrosative stress in the diaphragm of patients with COPD
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Time‐dependent changes in caspase‐3 activity and heat shock protein 25 after spinal cord transection in adult rats
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Nitric oxide production in the ventilatory muscles in response to acute resistive loading
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Diaphragmatic Fatigue and High Intensity Exercise in Patients with Chronic Obstructive Pulmonary Disease.
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Inhibition of Na+K+-ATPase by phenoxyl radicals of etoposide (VP-16): role of sulfhydryls oxidation
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Peripheral Muscle Alterations in Non-COPD Smokers.
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Chronic Obstructive Pulmonary Disease: Capillarity and Fiber-Type Characteristics of Skeletal Muscle.
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The effect of pH and hypoxia on function and intracellular pH of the rat diaphragm
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Quadriceps Fatigue After Cycle Exercise in Patients with COPD Compared with Healthy Control Subjects.
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Vascular-Specific Growth Factor mRNA Levels in the Human Diaphragm
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Couillard A Maltais F Saey D 2003 Exercise-induced quadriceps oxidative stress and peripheral muscle dysfunction in COPD patients Am J Respir Crit Care Med 167 1664 9 12672647
Espinosa A Leiva A Pena M 2006 Myotube depolarization generates reactive oxygen species through NAD(P)H oxidase; ROS-elicited Ca2+ stimulates ERK, CREB, early genes J Cell Physiol 209 379 88 16897752
Kobzik L Stringer B Balligand JL 1995 Endothelial type nitric oxide synthase in skeletal muscle fibers:mitochondrial relationship Biochm Biophys Res Commun 211 375 81 7540837

Sorted by citations

An Official American Thoracic Society/European Respiratory Society Statement: Update on Limb Muscle Dysfunction in Chronic Obstructive Pulmonary Disease
Maltais, F., Decramer, M., Casaburi, R. H., Barreiro, E., Burelle, Y., Debigaré, R., Dekhuijzen, P. N. R., Franssen, F. M. E., Gayan‐Ramirez, G., Gea, J., et al. (2014) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.201402-0373st · Cited by 1,113 · see citing works
Self-citation
Regulation of SIRT1 in cellular functions: Role of polyphenols
Chung, S., Yao, H., Caito, S. W., Hwang, J., Arunachalam, G., & Rahman, I. (2010) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2010.05.003 · Cited by 651 · see citing works
Hypoxemia in patients with COPD: cause, effects, and disease progression
McNicholas, W. T., Kent, & Mitchell (2011) · International Journal of COPD · doi:10.2147/copd.s10611 · Cited by 454 · see citing works
COPD and its comorbidities: Impact, measurement and mechanisms
Negewo, N. A., Gibson, P. G., & McDonald, V. M. (2015) · Respirology · doi:10.1111/resp.12642 · Cited by 317 · see citing works
Consilience in sarcopenia of cirrhosis
Dasarathy, S. (2012) · Journal of Cachexia Sarcopenia and Muscle · doi:10.1007/s13539-012-0069-3 · Cited by 248 · see citing works
The Breathing, Thinking, Functioning clinical model: a proposal to facilitate evidence-based breathlessness management in chronic respiratory disease
Spathis, A., Booth, S., Moffat, C., Hurst, R., Ryan, R., Chin, C., & Burkin, J. (2017) · npj Primary Care Respiratory Medicine · doi:10.1038/s41533-017-0024-z · Cited by 226 · see citing works
“However, inactivity leads to muscle deconditioning, with reduced oxidative capacity, muscle fibre atrophy and fibre type shift from type 1 (oxidative) to type IIb (glycolytic) fibres.(35) This increases the demand on the respiratory system, and worsens breathlessness further.”
Background
Epigenetic effects of natural polyphenols: A focus on SIRT1‐mediated mechanisms
Owona, V. B. A., Ebrahimi, A., & Schluesener, H. J. (2013) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201300195 · Cited by 125 · see citing works
Impact of Resistance Training in Subjects With COPD: A Systematic Review and Meta-Analysis
Liao, W., Chen, J., Chen, X., Lin, L., Yan, H., Zhou, Y., & Chen, R. (2015) · Respiratory Care · doi:10.4187/respcare.03598 · Cited by 123 · see citing works
Protein Carbonylation in Skeletal Muscles: Impact on Function
Barreiro, E., & Hussain, S. N. A. (2010) · Antioxidants & Redox Signaling · doi:10.1089/ars.2009.2808 · Cited by 108 · see citing works
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Targeting oxidant-dependent mechanisms for the treatment of COPD and its comorbidities
Bernardo, I., Bozinovski, S., & Vlahos, R. (2015) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2015.08.005 · Cited by 108 · see citing works
Ultrasonographic Assessment of the Diaphragm in Chronic Obstructive Pulmonary Disease Patients: Relationships with Pulmonary Function and the Influence of Body Composition - A Pilot Study
Smargiassi, A., Inchingolo, R., Tagliaboschi, L., Berardino, A. D. M., Valente, S., & Corbo, G. M. (2014) · Respiration · doi:10.1159/000358564 · Cited by 90 · see citing works
Low pulmonary function is related with a high risk of sarcopenia in community-dwelling older adults: the Korea National Health and Nutrition Examination Survey (KNHANES) 2008–2011
Jeon, Y. K., Shin, M., Kim, M. H., Mok, J. H., Kim, S. S., Kim, B. H., Kim, S.-J., Kim, Y. K., Chang, J. H., Shin, Y. B., et al. (2015) · Osteoporosis International · doi:10.1007/s00198-015-3152-8 · Cited by 90 · see citing works
TNF-α-Induced NF-ΚB Activation Stimulates Skeletal Muscle Glycolytic Metabolism through Activation of HIF-1α
Remels, A. H. V., Gosker, H. R., Verhees, K. J. P., Langen, R. C. J., & Schols, A. M. W. J. (2015) · Endocrinology · doi:10.1210/en.2014-1591 · Cited by 82 · see citing works
The importance of components of pulmonary rehabilitation, other than exercise training, in COPD
Hill, K., Vogiatzis, I., & Burtin, C. (2013) · European Respiratory Review · doi:10.1183/09059180.00002913 · Cited by 81 · see citing works
Chronic obstructive pulmonary disease (COPD): Evaluation from clinical, immunological and bacterial pathogenesis perspectives
Hassett, D. J., Borchers, M. T., & Panos, R. J. (2014) · The Journal of Microbiology · doi:10.1007/s12275-014-4068-2 · Cited by 75 · see citing works
Satellite Cells Senescence in Limb Muscle of Severe Patients with COPD
Thériault, M., Paré, M., Maltais, F., & Debigaré, R. (2012) · PLoS ONE · doi:10.1371/journal.pone.0039124 · Cited by 71 · see citing works
Mitochondrial accumulation of doxorubicin in cardiac and diaphragm muscle following exercise preconditioning
Morton, A. B., Huertas, A. M., Hinkley, J. M., Ichinoseki‐Sekine, N., Christou, D. D., & Smuder, A. J. (2018) · Mitochondrion · doi:10.1016/j.mito.2018.02.005 · Cited by 70 · see citing works
Effects of whole body vibration training in patients with severe chronic obstructive pulmonary disease
Pleguezuelos, E., Pérez, M. E., Guirao, L., Samitier, B., Costea, M., Ortega, P., González, M. V., Carmen, A. D., Ovejero, L. Q., Moreno, E., et al. (2013) · Respirology · doi:10.1111/resp.12122 · Cited by 66 · see citing works
Comorbidity in chronic obstructive pulmonary disease
Negewo, N. A., McDonald, V. M., & Gibson, P. G. (2015) · Respiratory Investigation · doi:10.1016/j.resinv.2015.02.004 · Cited by 66 · see citing works
Is the aging process accelerated in chronic obstructive pulmonary disease?
Lee, J., Sandford, A. J., Man, P., & Sin, D. D. (2010) · Current Opinion in Pulmonary Medicine · doi:10.1097/mcp.0b013e328341cead · Cited by 65 · see citing works
Correlation between Limb Muscle Endurance, Strength, and Functional Capacity in People with Chronic Obstructive Pulmonary Disease
Nyberg, A., Törnberg, A., & Wadell, K. (2016) · Physiotherapy Canada · doi:10.3138/ptc.2014-93 · Cited by 61 · see citing works
COPD elicits remodeling of the diaphragm and vastus lateralis muscles in humans
Levine, S., Bashir, M. H., Clanton, T. L., Powers, S. K., & Singhal, S. K. (2012) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01121.2012 · Cited by 61 · see citing works
Expression and Functional Significance of Nicotinamide N-methyl Transferase in Skeletal Muscles of Patients with Chronic Obstructive Pulmonary Disease
Kim, H. C., Mofarrahi, M., Vassilakopoulos, T., Maltais, F., Sigala, I., Debigaré, R., Bellenis, I., & Hussain, S. N. A. (2010) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.200906-0936oc · Cited by 61 · see citing works
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Methods and Applications in Respiratory Physiology: Respiratory Mechanics, Drive and Muscle Function in Neuromuscular and Chest Wall Disorders
Patel, N., Chong, K., & Baydur, A. (2022) · Frontiers in Physiology · doi:10.3389/fphys.2022.838414 · Cited by 59 · see citing works
Low-level phototherapy to improve exercise capacity and muscle performance: a systematic review and meta-analysis
Nampo, F. K., Cavalheri, V., Soares, F. D. S., Ramos, S. D. P., & Camargo, E. A. (2016) · Lasers in Medical Science · doi:10.1007/s10103-016-1977-9 · Cited by 57 · see citing works
Sabinene Prevents Skeletal Muscle Atrophy by Inhibiting the MAPK–MuRF-1 Pathway in Rats
Ryu, Y., Lee, D., Jung, S. H., Lee, K.-J., Jin, H., Kim, S. J., Lee, H. M., Kim, B., & Won, K. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20194955 · Cited by 53 · see citing works
Chronic obstructive pulmonary disease - diagnosis and management of stable disease; a personalized approach to care, using the treatable traits concept based on clinical phenotypes. Position paper of the Czech Pneumological and Phthisiological Society
Zatloukal, J., Brat, K., Neumannová, K., Voláková, E., Hejduk, K., Kočová, E., Kudela, O., Kopecký, M., Plutinský, M., & Koblížek, V. (2020) · Biomedical Papers · doi:10.5507/bp.2020.056 · Cited by 49 · see citing works
A systematic review and meta-analysis of the effectiveness of virtual reality as an exercise intervention for individuals with a respiratory condition
Condon, C. N., Lam, W. T., Mosley, C., & Gough, S. (2020) · Advances in Simulation · doi:10.1186/s41077-020-00151-z · Cited by 47 · see citing works
Hypoxia Aggravates Inactivity-Related Muscle Wasting
Debevec, T., Ganse, B., Mittag, U., Eiken, O., Mekjavić, I. B., & Rittweger, J. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.00494 · Cited by 47 · see citing works
Mass and Fat Infiltration of Intercostal Muscles Measured by CT Histogram Analysis and Their Correlations with COPD Severity
Park, M. J., Cho, J. M., Jeon, K. N., Bae, K. S., Kim, H. C., Choi, D. S., Na, J. B., Choi, H. C., Choi, H. Y., Kim, J. E., et al. (2014) · Academic Radiology · doi:10.1016/j.acra.2014.02.003 · Cited by 43 · see citing works
Swallow and Aspiration in Chronic Obstructive Pulmonary Disease
Cvejic, L., & Bardin, P. G. (2018) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.201804-0704pp · Cited by 43 · see citing works
Ultrasound Evaluation of Diaphragm Force Reserve in Patients with Chronic Obstructive Pulmonary Disease
Rittayamai, N., Chuaychoo, B., Tscheikuna, J., Dres, M., Goligher, E. C., & Brochard, L. J. (2020) · Annals of the American Thoracic Society · doi:10.1513/annalsats.202002-129oc · Cited by 43 · see citing works
Smoking cessation‐related weight gain—beneficial effects on muscle mass, strength and bone health
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Severe COPD Alters Muscle Fiber Conduction Velocity During Knee Extensors Fatiguing Contraction
Boccia, G., Coratella, G., Dardanello, D., Rinaldo, N., Lanza, M., Schena, F. F., & Rainoldi, A. (2016) · COPD Journal of Chronic Obstructive Pulmonary Disease · doi:10.3109/15412555.2016.1139561 · Cited by 41 · see citing works
Prevalence of quadriceps muscle weakness in patients with COPD and its association with disease severity
Kharbanda, Krishnan, S. K., & Ramakrishna, A. (2015) · International Journal of COPD · doi:10.2147/copd.s87791 · Cited by 37 · see citing works
Clinical importance of cross‐sectional area of intercostal muscles in patients with chronic obstructive pulmonary disease
Ju, S., Lee, S. J., Park, M. J., Cho, Y. J., Jeong, Y. Y., Jeon, K. N., Bae, K., Lee, J. D., & Kim, H. C. (2017) · The Clinical Respiratory Journal · doi:10.1111/crj.12609 · Cited by 35 · see citing works
Functional capacity, physical activity, and quality of life in hypoxemic patients with chronic obstructive pulmonary disease
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Physical and Functional Impairment During and After Hospitalization in Subjects With Severe COPD Exacerbation
Torres‐Sánchez, I., Martos, I. C., Díaz-Pelegrina, A., Valenza‐Demet, G., Moreno-Ramírez, M. P., & Valenza, M. C. (2016) · Respiratory Care · doi:10.4187/respcare.04597 · Cited by 35 · see citing works
Relationship between pulmonary function and physical performance among community‐living people: results from Look‐up 7+ study
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Physical Activity Patterns in Patients in Different Stages of Chronic Obstructive Pulmonary Disease
Eliason, G., Zakrisson, A., Piehl‐Aulin, K., & Hurtig‐Wennlöf, A. (2011) · COPD Journal of Chronic Obstructive Pulmonary Disease · doi:10.3109/15412555.2011.605403 · Cited by 32 · see citing works
MuRF-1 and Atrogin-1 Protein Expression and Quadriceps Fiber Size and Muscle Mass in Stable Patients with COPD
Natanek, S. A., Riddoch-Contreras, J., Marsh, G. S., Hopkinson, N. S., Moxham, J., Man, W. D.-C., Kemp, P. R., & Polkey, M. I. (2013) · COPD: Journal of Chronic Obstructive Pulmonary Disease · doi:10.3109/15412555.2013.781577 · Cited by 32 · see citing works
Clinical, physiologic, and radiographic factors contributing to development of hypoxemia in moderate to severe COPD: a cohort study
the COPDGene Investigators, Wells, J. M., Estépar, R. S. J., McDonald, M., Bhatt, S. P., Díaz, A. A., Bailey, W. C., Jacobson, F. L., Dransfield, M. T., Washko, G. R., et al. (2016) · BMC Pulmonary Medicine · doi:10.1186/s12890-016-0331-0 · Cited by 32 · see citing works
Validation of an active shape model-based semi-automated segmentation algorithm for the analysis of thigh muscle and adipose tissue cross-sectional areas
Kemnitz, J., Eckstein, F., Culvenor, A. G., Ruhdorfer, A., Dannhauer, T., Ring‐Dimitriou, S., Sänger, A. M., & Wirth, W. (2017) · Magnetic Resonance Materials in Physics Biology and Medicine · doi:10.1007/s10334-017-0622-3 · Cited by 32 · see citing works
Prevalence of osteoarthritis in individuals with COPD: a systematic review
Wshah, A., Guilcher, S. J. T., Goldstein, R. S., & Brooks, D. (2018) · International Journal of COPD · doi:10.2147/copd.s158614 · Cited by 31 · see citing works
Multidimensional indices in the assessment of chronic obstructive pulmonary disease
Corlăteanu, A., Plahotniuc, A., Corlateanu, O., Botnaru, V., Bikov, A., Mathioudakis, A. G., Covanţev, S., & Siafakas, N. M. (2021) · Respiratory Medicine · doi:10.1016/j.rmed.2021.106519 · Cited by 30 · see citing works
Breathlessness – current and emerging mechanisms, measurement and management: A discussion from an European Association of Palliative Care workshop
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Active Video Games as an Adjunct to Pulmonary Rehabilitation of Patients With Chronic Obstructive Pulmonary Disease
Wang, Y., Liu, X., Ma, R., Yin, Y., Yang, Z., Cao, H., & Xie, J. (2019) · American Journal of Physical Medicine & Rehabilitation · doi:10.1097/phm.0000000000001341 · Cited by 28 · see citing works
Vitamin D status is associated with muscle strength and quality of life in patients with COPD: a seasonal prospective observation study
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Skeletal Muscle Dysfunction in Chronic Obstructive Pulmonary Disease: A Statement of the American Thoracic Society and European Respiratory Society
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Skeletal Muscle Dysfunction
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Authors: Hussain, S., Cheol, K., & Mofarrahi, M.
Affiliations: McGill University Health Centre (CA)
Gyeongsang National University (KR)
Corresponding author: Hussain, Sabah
ORCID: Hussain, Sabah
Venue: International Journal of Chronic Obstructive Pulmonary Disease
Publisher: Informa UK Limited
Published: 2008-12
Volume: Volume 3
Issue: 4
Pages: 637-658
ISSN: 1176-9106 (ISSN-L)
1178-2005
DOI: 10.2147/copd.s4480
PMC: PMC2650609
OpenAlex: W2109041485
Cited by: 224
References: 190
Citations by year: 2026: 9 · 2025: 5 · 2024: 10 · 2023: 16 · 2022: 12 · 2021: 11 · 2020: 14 · 2019: 12 · 2018: 20 · 2017: 17 · 2016: 14 · 2015: 22 · 2014: 19 · 2013: 15 · 2012: 5
FWCI: 1.22
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by-nc
creativecommons.org/licenses/by-nc/3.0/ (unspecified)
Locations: International Journal of COPD (publishedVersion, cc-by-nc)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Chronic Obstructive Pulmonary Disease (COPD) Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
Health Sciences › Medicine › Physiology › Nutrition and Health in Aging
Keywords: chronic obstructive pulmonary disease, skeletal muscle dysfunction, exercise capacity, systemic inflammation, nutrient depletion, hypoxemia, oxidative stress, nitrosative stress, protein degradation, quality of life, exertional dyspnea, muscle atrophy
MeSH terms: Animals, Humans, Muscular Atrophy, Quality of Life, Pulmonary Ventilation, Respiratory Muscles, Risk Factors, Work of Breathing, Exercise Tolerance, Muscle, Skeletal, Muscle Fibers, Skeletal, Muscle Fatigue, Pulmonary Disease, Chronic Obstructive, Muscle Strength

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Skeletal muscle dysfunction in patients with chronic obstructive pulmonary disease

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