Quadriceps Exercise Intolerance in Patients with Chronic Obstructive Pulmonary Disease: The Potential Role of Altered Skeletal Muscle Mitochondrial Respiration
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This study sought to determine if qualitative alterations in skeletal muscle mitochondrial respiration, associated with decreased mitochondrial efficiency, contribute to exercise intolerance in patients with chronic obstructive pulmonary disease (COPD). Using permeabilized muscle fibers from the vastus lateralis of 13 patients with COPD and 12 healthy controls, complex I (CI) and complex II (CII)-driven State 3 mitochondrial respiration were measured separately (State 3:CI and State 3:CII) and in combination (State 3:CI+CII). State 2 respiration was also measured. Exercise tolerance was assessed by knee extensor exercise (KE) time to fatigue. Per milligram of muscle, State 3:CI+CII and State 3:CI were reduced in COPD ( P < 0.05), while State 3:CII and State 2 were not different between groups. To determine if this altered pattern of respiration represented qualitative changes in mitochondrial function, respiration states were examined as percentages of peak respiration (State 3:CI+CII), which revealed altered contributions from State 3:CI (Con 83.7 ± 3.4, COPD 72.1 ± 2.4%Peak, P < 0.05) and State 3:CII (Con 64.9 ± 3.2, COPD 79.5 ± 3.0%Peak, P < 0.05) respiration, but not State 2 respiration in COPD. Importantly, a diminished contribution of CI-driven respiration relative to the metabolically less-efficient CII-driven respiration (CI/CII) was also observed in COPD (Con 1.28 ± 0.09, COPD 0.81 ± 0.05, P < 0.05), which was related to exercise tolerance of the patients ( r = 0.64, P < 0.05). Overall, this study indicates that COPD is associated with qualitative alterations in skeletal muscle mitochondria that affect the contribution of CI and CII-driven respiration, which potentially contributes to the exercise intolerance associated with this disease.
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Gifford and colleagues confirmed their observations in 2017 on a different cohort of COPD patients matched to healthy controls based on the same physical activity, observing a diminished state 3 CI-driven respiration and a trend to a lower state 3:CI+CII driven respiration.
“The same authors confirmed their observations in 2017 on a different cohort of COPD patients matched to healthy controls based on the same physical activity, in order to avoid disuse bias. They observed a diminished state 3 CI-driven respiration, and a trend to a lower state 3:CI+CII driven respiration.”
From Main Pathogenic Mechanisms and Recent Advances in COPD Peripheral Skeletal Muscle Wasting (2023) · cites this paper as [101]
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Experimental — accuracy not yet measuredNormalization of respiration with respect to citrate synthase activity again revealed no differences in any state 3 or state 2 respiration between COPD and healthy.
“However, the normalization of respiration with respect to the citrate synthase activity again revealed no differences in any state 3 or state 2 respiration between COPD and healthy”
From Main Pathogenic Mechanisms and Recent Advances in COPD Peripheral Skeletal Muscle Wasting (2023) · cites this paper as [101]
The Mitochondrial respiration and muscle characteristics section (page unavailable) reports no group difference in State 2 respiration, and the reported results also show no difference in State 3:CII. However, the Methods describe normalization to muscle weight or peak respiration, not citrate synthase activity; State 3:CI differs between groups under those analyses. The source therefore does not support the claim that citrate-synthase normalization eliminated differences in every State 3 measure. (LLM, conf=0.86)
Experimental — accuracy not yet measuredGifford and colleagues concluded that the reduction in state 3:CI+CII respiration was largely driven by diminished CI-driven respiration rather than CII-driven respiration.
“they concluded that this reduction was largely driven by diminished CI-driven respiration rather than CII-driven respiration.”
From Main Pathogenic Mechanisms and Recent Advances in COPD Peripheral Skeletal Muscle Wasting (2023) · cites this paper as [101]
Gifford and colleagues observed a reduction in state 3:CI+CII respiration in COPD patients compared to healthy controls.
“Gifford and colleagues observed a reduction in state 3:CI+CII respiration in COPD patients compared to healthy controls [101].”
From Main Pathogenic Mechanisms and Recent Advances in COPD Peripheral Skeletal Muscle Wasting (2023) · cites this paper as [101]
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Cites
Celli, B. R., MacNee, W., Agustí, A. G. N., Anzueto, A. R., Berg, B., Buist, A. S., Calverley, P. M., Chavannes, N. H., Dillard, T. A., Fahy, B. F., et al. (2004) · European Respiratory Journal · doi:10.1183/09031936.04.00014304 · Cited by 4,414 · see citing works
How Many Steps/Day Are Enough?: Preliminary Pedometer Indices for Public Health
Tudor-Locke, C., & Bassett, D. R. (2004) · Sports Medicine · doi:10.2165/00007256-200434010-00001 · Cited by 2,054 · see citing works
Systemic manifestations and comorbidities of COPD
Barnes, P. J., & Celli, B. R. (2009) · European Respiratory Journal · doi:10.1183/09031936.00128008 · Cited by 1,818 · see citing works
Maximal perfusion of skeletal muscle in man.
Andersen, P., & Saltin, B. (1985) · The Journal of Physiology · doi:10.1113/jphysiol.1985.sp015794 · Cited by 1,250 · see citing works
Pesta, D. H., & Gnaiger, E. (2011) · Methods in molecular biology · doi:10.1007/978-1-61779-382-0_3 · Cited by 1,005 · see citing works
Physiological functions of the mitochondrial uncoupling proteins UCP2 and UCP3
Brand, M. D., & Esteves, T. C. (2005) · Cell Metabolism · doi:10.1016/j.cmet.2005.06.002 · Cited by 785 · see citing works
Improvements in Speed-Based Gait Classifications Are Meaningful
Schmid, A. A., Duncan, P. W., Studenski, S. A., Lai, S. M., Richards, L. G., Perera, S., & Wu, S. S. (2007) · Stroke · doi:10.1161/strokeaha.106.475921 · Cited by 655 · see citing works
Bloemberg, D., & Quadrilatero, J. (2012) · PLoS ONE · doi:10.1371/journal.pone.0035273 · Cited by 613 · see citing works
Consequences of exercise-induced respiratory muscle work
Dempsey, J. A., Romer, L., Rodman, J., Miller, J., & Smith, C. (2006) · Respiratory Physiology & Neurobiology · doi:10.1016/j.resp.2005.12.015 · Cited by 398 · see citing works
P/O ratios of mitochondrial oxidative phosphorylation
Hinkle, P. C. (2004) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2004.09.004 · Cited by 336 · see citing works
Validity of physical activity monitors during daily life in patients with COPD
Rabinovich, R., Louvaris, Z., Raste, Y., Langer, D., Remoortel, H. V., Giavedoni, S., Burtin, C., Regueiro, E. M. G., Vogiatzis, I., Hopkinson, N. S., et al. (2013) · European Respiratory Journal · doi:10.1183/09031936.00134312 · Cited by 289 · see citing works
High muscle blood flow in man: is maximal O2 extraction compromised?
Richardson, R. S., Poole, D. C., Knight, D. R., Kurdak, S. S., Hogan, M. C., Grassi, B., Johnson, E. C., Kendrick, K., Erickson, B. K., & Wagner, P. D. (1993) · Journal of Applied Physiology · doi:10.1152/jappl.1993.75.4.1911 · Cited by 264 · see citing works
Self-citationWhipp, B. J., & Wasserman, K. (1969) · Journal of Applied Physiology · doi:10.1152/jappl.1969.26.5.644 · Cited by 259 · see citing works
Determinants of maximal exercise VO2 during single leg knee-extensor exercise in humans
Richardson, R. S., Knight, D. R., Poole, D. C., Kurdak, S. S., Hogan, M. C., Grassi, B., & Wagner, P. D. (1995) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1995.268.4.h1453 · Cited by 176 · see citing works
Self-citationRichardson, R. S., Leek, B. T., Gavin, T. P., Haseler, L. J., Mudaliar, S. R. D., Henry, R. R., Mathieu-Costello, O. A., & Wagner, P. D. (2003) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.200305-627oc · Cited by 175 · see citing works
Self-citationAbnormal Mitochondrial Function in Locomotor and Respiratory Muscles of COPD Patients
Puente-Maestu, L., Pérez-Parra, J., Godoy, R., Moreno, N., Tejedor, A., González-Aragoneses, F., Bravo, J.-L., Villar Álvarez, F., Camaño, S., & Agustí, A. (2009) · European Respiratory Journal · doi:10.1183/09031936.00112408 · Cited by 172 · see citing works
Simvastatin Effects on Skeletal Muscle
Larsen, S., Stride, N., Hey-Mogensen, M., Hansen, C. N., Bang, L. E., Bundgaard, H., Nielsen, L. B., Helge, J. W., & Dela, F. (2013) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2012.09.036 · Cited by 165 · see citing works
Self-citationImpact of pulmonary system limitations on locomotor muscle fatigue in patients with COPD
Amann, M., Regan, M. S., Kobitary, M., Eldridge, M. W., Boutellier, U., Pegelow, D. F., & Dempsey, J. A. (2010) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00183.2010 · Cited by 150 · see citing works
Mitochondrial Dysfunction in COPD Patients with Low Body Mass Index
Rabinovich, R. A., Bastos, R., Ardite, E., Llinàs, L., Orozco-Levi, M., Gea, J., Vilaró, J., Barberà, J. A., Rodríguez-Roisin, R., Fernández-Checa, J. C., et al. (2007) · European Respiratory Journal · doi:10.1183/09031936.00086306 · Cited by 144 · see citing works
Daussin, F., Zoll, J., Ponsot, E., Dufour, S. P., Doutreleau, S., Lonsdorfer‐Wolf, E., Ventura‐Clapier, R., Mettauer, B., Piquard, F., Gény, B., et al. (2008) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01135.2007 · Cited by 106 · see citing works
Maximal exercise capacity and peripheral skeletal muscle function following lung transplantation
Lands, L. C., Smountas, A. A., Mesiano, G., Brosseau, L., Shennib, H., Charbonneau, M., & Gauthier, R. (1999) · The Journal of Heart and Lung Transplantation · doi:10.1016/s1053-2498(98)00027-8 · Cited by 106 · see citing works
Chronic corticosteroid administration causes mitochondrial dysfunction in skeletal muscle
Mitsui, T., Azuma, H., Nagasawa, M., Iuchi, T., Akaike, M., Odomi, M., & Matsumoto, T. (2002) · Journal of Neurology · doi:10.1007/s00415-002-0774-5 · Cited by 104 · see citing works
The Mitochondrial Phenotype of Peripheral Muscle in Chronic Obstructive Pulmonary Disease
Picard, M., Godin, R., Sinnreich, M., Baril, J., Bourbeau, J., Perrault, H., Taivassalo, T., & Burelle, Y. (2008) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.200807-1005oc · Cited by 95 · see citing works
Decreased mechanical efficiency in clinically stable patients with COPD
Baarends, E. M., Schols, A. M. W. J., Akkermans, M. A., & Wouters, E. F. �. (1997) · Thorax · doi:10.1136/thx.52.11.981 · Cited by 80 · see citing works
Bartels, M. N., Armstrong, H. F., Gerardo, R. E., Layton, A. M., Emmert‐Aronson, B. O., Sonett, J. R., & Arcasoy, S. M. (2011) · CHEST Journal · doi:10.1378/chest.10-2721 · Cited by 69 · see citing works
Effects of exercise on mitochondrial DNA content in skeletal muscle of patients with COPD
Puente‐Maestu, L., Lázaro, A., Tejedor, A., Camaño, S., Fuentes, M., Cuervo, M., Navarro, B., & Agustí, A. G. N. (2010) · Thorax · doi:10.1136/thx.2010.153031 · Cited by 68 · see citing works
High-intensity knee extensor training restores skeletal muscle function in COPD patients
Brønstad, E., Rognmo, Ø., Tjønna, A. E., Dedichen, H., Kirkeby‐Garstad, I., Haberg, A. K., Ingul, C. B., Wisløff, U., & Steinshamn, S. (2012) · European Respiratory Journal · doi:10.1183/09031936.00193411 · Cited by 66 · see citing works
Knower, M. T., Dunagan, D. P., Adair, N. E., & Robert Chin, Jr. (2001) · Archives of Internal Medicine · doi:10.1001/archinte.161.5.732 · Cited by 58 · see citing works
Layec, G., Venturelli, M., Jeong, E., & Richardson, R. S. (2014) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01120.2013 · Cited by 56 · see citing works
Self-citationLayec, G., Haseler, L. J., Hoff, J., & Richardson, R. S. (2011) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00835.2010 · Cited by 55 · see citing works
Self-citationAltered mitochondrial regulation in quadriceps muscles of patients with COPD
Naimi, A. I., Bourbeau, J., Perrault, H., Baril, J., Wright‐Paradis, C., Rossi, A. M., Taivassalo, T., Sheel, A. W., Rabøl, R., Dela, F., et al. (2010) · Clinical Physiology and Functional Imaging · doi:10.1111/j.1475-097x.2010.00988.x · Cited by 51 · see citing works
Self-citationRossman, M. J., Garten, R. S., Groot, H. J., Reese, V. R., Zhao, J., Amann, M., & Richardson, R. S. (2013) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00360.2013 · Cited by 37 · see citing works
Self-citationOxygen delivery-utilization mismatch in contracting locomotor muscle in COPD: peripheral factors
Medeiros, W. M., Fernandes, M. C. T., Azevedo, D. P., de Freitas, F. F. M., Amorim, B. C., Chiavegato, L. D., Hirai, D. M., O’Donnell, D. E., & Neder, J. A. (2014) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00404.2014 · Cited by 25 · see citing works
Layec, G., Haseler, L. J., & Richardson, R. S. (2011) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00986.2011 · Cited by 20 · see citing works
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Li, Y., & Yao, H. (2016) · British Journal of Pharmacology · doi:10.1111/bph.13518 · Cited by 138 · see citing works
Choudhury, G., & MacNee, W. (2016) · COPD Journal of Chronic Obstructive Pulmonary Disease · doi:10.1080/15412555.2016.1214948 · Cited by 88 · see citing works
Frailty in Pulmonary and Critical Care Medicine
Singer, J. P., Lederer, D. J., & Baldwin, M. R. (2016) · Annals of the American Thoracic Society · doi:10.1513/annalsats.201512-833fr · Cited by 86 · see citing works
Main Pathogenic Mechanisms and Recent Advances in COPD Peripheral Skeletal Muscle Wasting
Henrot, P., Dupin, I., Schilfarth, P., Esteves, P., Blervaque, L., Zysman, M., Gouzi, F., Hayot, M., Pomiès, P., & Berger, P. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24076454 · Cited by 85 · see citing works
“Finally, Gifford and colleagues observed a reduction in state 3:CI+CII respiration in COPD patients compared to healthy controls [101].”
BackgroundFunctional, proteomic and bioinformatic analyses of Nrf2- and Keap1- null skeletal muscle
Gao, L., Kumar, V., Vellichirammal, N. N., Park, S., Rudebush, T. L., Yu, L., Son, W., Pekas, E. J., Wafi, A. M., Hong, J., et al. (2020) · The Journal of Physiology · doi:10.1113/jp280176 · Cited by 58 · see citing works
Self-citationFrailty assessment in older adults with chronic obstructive respiratory diseases
Guan, C., & Niu, H. (2018) · Clinical Interventions in Aging · doi:10.2147/cia.s173239 · Cited by 57 · see citing works
Acute High-Intensity Exercise Impairs Skeletal Muscle Respiratory Capacity
Layec, G., Blain, G. M., Rossman, M. J., Park, S., Hart, C. R., Trinity, J. D., Gifford, J. R., Sidhu, S. K., Weavil, J. C., Hureau, T. J., et al. (2018) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000001735 · Cited by 55 · see citing works
Self-citationExercise training improves vascular mitochondrial function
Park, S., Rossman, M. J., Gifford, J. R., Bharath, L. P., Bauersachs, J. K., Richardson, R. S., Abel, E. D., Symons, J. D., & Riehle, C. (2016) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00751.2015 · Cited by 51 · see citing works
Self-citationBroxterman, R. M., Hoff, J., Wagner, P. D., & Richardson, R. S. (2019) · The Journal of Physiology · doi:10.1113/jp279135 · Cited by 48 · see citing works
Self-citationResveratrol and metabolic health in COPD: A proof-of-concept randomized controlled trial
Beijers, R. J. H. C. G., Gosker, H. R., Sanders, K. J. C., de Theije, C. C., KELDERS, M. C. J. M., Clarke, G. A., Cryan, J. F., van den Borst, B., & Schols, A. M. W. J. (2020) · Clinical Nutrition · doi:10.1016/j.clnu.2020.01.002 · Cited by 48 · see citing works
Locomotor Muscles in COPD: The Rationale for Rehabilitative Exercise Training
Marillier, M., Bernard, A., Vergès, S., & Neder, J. A. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2019.01590 · Cited by 46 · see citing works
Altered skeletal muscle mitochondrial phenotype in COPD: disease vs. disuse
Gifford, J. R., Trinity, J. D., Kwon, O.-S., Layec, G., Garten, R. S., Park, S., Nelson, A. D., & Richardson, R. S. (2017) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00788.2017 · Cited by 45 · see citing works
Self-citationHart, C. R., Layec, G., Trinity, J. D., Kwon, O. S., Zhao, J., Reese, V. R., Gifford, J. R., & Richardson, R. S. (2018) · Experimental Physiology · doi:10.1113/ep086905 · Cited by 44 · see citing works
Self-citationResveratrol for patients with chronic obstructive pulmonary disease
Beijers, R. J. H. C. G., Gosker, H. R., & Schols, A. M. W. J. (2017) · Current Opinion in Clinical Nutrition & Metabolic Care · doi:10.1097/mco.0000000000000444 · Cited by 41 · see citing works
Ives, S. J., Zaleski, K. S., Slocum, C., Escudero, D., Sheridan, C., Legesse, S., Vidal, K., Lagalwar, S., & Reynolds, T. (2020) · Physiological Reports · doi:10.14814/phy2.14630 · Cited by 38 · see citing works
The Relevance of Limb Muscle Dysfunction in Chronic Obstructive Pulmonary Disease
Bui, K.-L., Nyberg, A., Rabinovich, R., Saey, D., & Maltais, F. (2019) · Clinics in Chest Medicine · doi:10.1016/j.ccm.2019.02.013 · Cited by 32 · see citing works
Skeletal muscle mitochondrial adaptations induced by long-term cigarette smoke exposure
Decker, S. T., Kwon, O., Zhao, J., Hoidal, J. R., Heuckstadt, T., Richardson, R. S., Sanders, K. A., & Layec, G. (2021) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00544.2020 · Cited by 24 · see citing works
Self-citationWang, Z., Deng, M., Xu, W., Li, C., Zheng, Z., Li, J., Liao, L., Zhang, Q., Bian, Y., Li, R., et al. (2024) · Redox Biology · doi:10.1016/j.redox.2024.103434 · Cited by 22 · see citing works
Vascular mitochondrial respiratory function: the impact of advancing age
Park, S. H., Kwon, O. S., Park, S., Weavil, J. C., Andtbacka, R. H. I., Hyngstrom, J. R., Reese, V. R., & Richardson, R. S. (2018) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00324.2018 · Cited by 21 · see citing works
Self-citationKwon, O. S., Decker, S. T., Zhao, J., Hoidal, J. R., Heuckstadt, T., Sanders, K. A., Richardson, R. S., & Layec, G. (2022) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2022.12.089 · Cited by 20 · see citing works
Self-citationLayec, G., Hart, C. R., Trinity, J. D., Kwon, O.-S., Rossman, M. J., Broxterman, R. M., Fur, Y. L., Jeong, E., & Richardson, R. S. (2017) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00462.2016 · Cited by 20 · see citing works
Self-citationOral N-acetylcysteine and exercise tolerance in mild chronic obstructive pulmonary disease
Hirai, D. M., Jones, J. H., Zelt, J. T., da Silva, M. L., Bentley, R. F., Edgett, B. A., Gurd, B. J., Tschakovsky, M. E., O’Donnell, D. E., & Neder, J. A. (2017) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00990.2016 · Cited by 16 · see citing works
Azevedo, D. P., Medeiros, W. M., de Freitas, F. F. M., Amorim, C. F., Gimenes, A. C., Neder, J. A., & Chiavegato, L. D. (2016) · European Journal of Applied Physiology · doi:10.1007/s00421-016-3442-7 · Cited by 15 · see citing works
Whole-body and muscle responses to aerobic exercise training and withdrawal in ageing and COPD
Latimer, L. E., Constantin-Teodosiu, D., Popat, B., Constantin, D., Houchen-Wolloff, L., Bolton, C. E., Steiner, M. C., & Greenhaff, P. L. (2022) · European Respiratory Journal · doi:10.1183/13993003.01507-2021 · Cited by 14 · see citing works
Moezy, A., Erfani, A., Mazaherinezhad, A., & Mousavi, S. A. (2018) · Medical Journal of the Islamic Republic of Iran · doi:10.14196/mjiri.32.49 · Cited by 14 · see citing works
Khattri, R. B., Thome, T., Fitzgerald, L. F., Wohlgemuth, S. E., Hepple, R. T., & RYAN, T. E. (2022) · Toxics · doi:10.3390/toxics10030140 · Cited by 14 · see citing works
Abdellaoui, A., Gouzi, F., Notarnicola, C., Bourret, A., Suc, A., Laoudj‐Chenivesse, D., Héraud, N., Mercier, J. G., PREFAUT, C. G., Hayot, M., et al. (2025) · Acta Physiologica · doi:10.1111/apha.70079 · Cited by 12 · see citing works
Foulkes, S., Wagner, P. D., Wang, J., Gerche, A. L., & Haykowsky, M. J. (2024) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00918.2023 · Cited by 11 · see citing works
Balnis, J., Tufts, A., Jackson, E. L., Drake, L. A., Singer, D. V., Lacomis, D., Lee, C. G., Elias, J. A., Doles, J. D., Maher, L. J., et al. (2024) · Science Advances · doi:10.1126/sciadv.ado8549 · Cited by 13 · see citing works
Medina, L. A. R., Oliveira, M. F., dos Santos, R. D. C. L., de Souza, A. S., Mazzuco, A., Sperandio, P. A., Alencar, M. C. N., Arbex, F. F., Neder, J. A., & Medeiros, W. M. (2024) · Acta cardiologica. Supplementum · doi:10.1080/00015385.2024.2319955 · Cited by 10 · see citing works
Revisiting the Single-Visit Protocol for Determining the Electromyographic Fatigue Threshold
Khan, F. L., Lawal, J. M., Kapture, D. O., Swingle, J. D., & Malek, M. H. (2017) · The Journal of Strength and Conditioning Research · doi:10.1519/jsc.0000000000002274 · Cited by 10 · see citing works
Lewis, M. T., Blain, G. M., Hart, C. R., Layec, G., Rossman, M. J., Park, S., Trinity, J. D., Gifford, J. R., Sidhu, S. K., Weavil, J. C., et al. (2021) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00158.2021 · Cited by 9 · see citing works
Self-citationSanders, K. J. C., Ash, S. Y., Washko, G. R., Mottaghy, F. M., & Schols, A. M. W. J. (2017) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00143.2017 · Cited by 9 · see citing works
Chung, S., Nelson, M. D., Hamaoka, T., Jacobs, R. A., Pearson, J., Subudhi, A. W., Jenkins, N. T., Bartlett, M. F., Fitzgerald, L. F., Miehm, J. D., et al. (2018) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00857.2017 · Cited by 7 · see citing works
Decker, S. T., Alexandrou-Majaj, N., & Layec, G. (2023) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2023.148973 · Cited by 5 · see citing works
Self-citationSymmorphosis in patients with chronic heart failure?
Gifford, J. R., Weavil, J. C., & Nelson, A. D. (2016) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00773.2016 · Cited by 4 · see citing works
Self-citationRuple, B. A., Park, S. H., Craig, J. C., Lewis, M. T., Trinity, J. D., Richardson, R. S., & Broxterman, R. M. (2025) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2025.149568 · Cited by 1 · see citing works
Self-citationOberholzer, L., Mølmen, K. S., Hammarström, D., Slettaløkken, G., Lundby, A. M., Rønnestad, B. R., Ellefsen, S., & Lundby, C. (2022) · JCSM Rapid Communications · doi:10.1002/rco2.58 · Cited by 1 · see citing works
Machin, D. R., Islam, M. T., Malouf, A., Nguyen, D. C., Sabouri, M., Boulos, M., Horn, A. G., Schulze, K. M., Layec, G., Lesniewski, L. A., et al. (2025) · Aging · doi:10.18632/aging.206313 · Cited by 1 · see citing works
Self-citationLower-Limb Muscle Impairments in Patients with COPD: An Overview of the Past Decade
Brauwers, B., Spruit, M. A., Franssen, F. M. E., Vaes, A. W., & Machado, F. V. C. (2026) · Cells · doi:10.3390/cells15030220
- Authors
- Gifford, J. R., Trinity, J. D., Layec, G., Garten, R. S., Park, S.-Y., Rossman, M. J., Larsen, S., Dela, F., & Richardson, R. S.
- Affiliations
- University of Utah (US)
- Geriatric Research, Education, and Clinical Center, Salt Lake City Veterans Affairs Medical Center, Salt Lake City, Utah;
- University of Copenhagen (DK)
- Corresponding author
- Richardson, Russell S.
- ORCID
- Venue
- Journal of Applied Physiology
- Publisher
- American Physiological Society
- Published
- 2015-10-15
- Volume
- 119
- Issue
- 8
- Pages
- 882-888
- ISSN
- 0161-7567 (ISSN-L)
- 8750-7587
- 1522-1601
- PMC
- PMC4610006
- OpenAlex
- W1943234789
- Cited by
- 40
- References
- 34
- Citations by year
- 2026: 1 · 2025: 3 · 2024: 4 · 2023: 2 · 2022: 3 · 2021: 3 · 2020: 4 · 2019: 2 · 2018: 6 · 2017: 6 · 2016: 6
- FWCI
- 2.61
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Applied Physiology (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- DigitalCommons@UNO (submittedVersion)
- Research at the University of Copenhagen (University of Copenhagen) (submittedVersion)
- Funders
- HHS | NIH | National Heart, Lung, and Blood Institute (NHBLI) (HL-09830)
- Tobacco-Related Disease Research Program (TRDRP) (15RT-0100)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Health Sciences › Medicine › Complementary and alternative medicine › Cardiovascular and exercise physiology
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Chronic Obstructive Pulmonary Disease (COPD) Research
- Keywords
- chronic obstructive pulmonary disease, exercise intolerance, complex I, complex II, state 3 respiration, vastus lateralis, mitochondrial efficiency, quadriceps
- MeSH terms
- Aged, Female, Humans, Male, Middle Aged, Mitochondria, Muscle, Oxygen Consumption, Exercise, Exercise Tolerance, Pulmonary Disease, Chronic Obstructive, Electron Transport Complex II, Electron Transport Complex I, Quadriceps Muscle
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