Hemodynamic and neuromuscular basis of reduced exercise capacity in patients with end-stage renal disease.
Chronic kidney disease
Exercise
Fatigue
Hemodynamic
Journal
European journal of applied physiology
ISSN: 1439-6327
Titre abrégé: Eur J Appl Physiol
Pays: Germany
ID NLM: 100954790
Informations de publication
Date de publication:
19 Feb 2024
19 Feb 2024
Historique:
received:
20
05
2023
accepted:
27
01
2024
medline:
20
2
2024
pubmed:
20
2
2024
entrez:
20
2
2024
Statut:
aheadofprint
Résumé
The present study aimed to characterize the exercise-induced neuromuscular fatigue and its possible links with cerebral and muscular oxygen supply and utilization to provide mechanistic insights into the reduced exercise capacity characterizing patients with end-stage renal disease (ESRD). Thirteen patients with ESRD and thirteen healthy males (CTR group) performed a constant-force sustained isometric contraction at 50% of their maximal voluntary isometric contraction (MVC) until exhaustion. Quadriceps muscle activation during exercise was estimated from vastus lateralis, vastus medialis, and rectus femoris EMG. Central and peripheral fatigue were quantified via changes in pre- to postexercise quadriceps voluntary activation (ΔVA) and quadriceps twitch force (ΔQ ESRD patients demonstrated lower exercise time to exhaustion than that of CTR (88.8 ± 15.3 s and 119.9 ± 14.6 s, respectively, P < 0.01). Following the exercise, MVC, Q These findings support cerebral hypoperfusion as a factor contributing to the reduction in exercise capacity characterizing ESRD patients.
Identifiants
pubmed: 38374473
doi: 10.1007/s00421-024-05427-0
pii: 10.1007/s00421-024-05427-0
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2024. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Allen DG, Lamb GD, Westerblad H (2008) Skeletal muscle fatigue: cellular mechanisms. Physiol Rev 88(1):287–332. https://doi.org/10.1152/physrev.00015.2007
doi: 10.1152/physrev.00015.2007
pubmed: 18195089
Amann M, Calbet JA (2008) Convective oxygen transport and fatigue. J Appl Physiol 104(3):861–870. https://doi.org/10.1152/japplphysiol.01008.2007
doi: 10.1152/japplphysiol.01008.2007
pubmed: 17962570
Ansdell P, Brownstein CG, Škarabot J, Hicks KM, Simoes DCM, Thomas K, Goodall S (2019) Menstrual cycle-associated modulations in neuromuscular function and fatigability of the knee extensors in eumenorrheic women. J Appl Physiol 126(6):1701–1712. https://doi.org/10.1152/japplphysiol.01041.2018
doi: 10.1152/japplphysiol.01041.2018
pubmed: 30844334
Arnold R, Issar T, Krishnan AV, Pussell BA (2016) Neurological complications in chronic kidney disease. JRSM Cardiovasc Dis 5:2048004016677687. https://doi.org/10.1177/2048004016677687
doi: 10.1177/2048004016677687
pubmed: 27867500
pmcid: 5102165
Arnold R, Pianta TJ, Pussell BA, Endre Z, Kiernan MC, Krishnan AV (2019) Potassium control in chronic kidney disease: implications for neuromuscular function. Intern Med J 49(7):817–825. https://doi.org/10.1111/imj.14114
doi: 10.1111/imj.14114
pubmed: 30230667
Arnold R, Pianta TJ, Issar T, Kirby A, Scales CMK, Kwai NCG, Krishnan AV (2022) Peripheral neuropathy: an important contributor to physical limitation and morbidity in stages 3 and 4 chronic kidney disease. Nephrol Dial Transplant 37(4):713–719. https://doi.org/10.1093/ndt/gfab043
doi: 10.1093/ndt/gfab043
pubmed: 33576810
Baecke JA, Burema J, Frijters JE (1982) A short questionnaire for the measurement of habitual physical activity in epidemiological studies. Am J Clin Nutr 36(5):936–942. https://doi.org/10.1093/ajcn/36.5.936
doi: 10.1093/ajcn/36.5.936
pubmed: 7137077
Bigland-Ritchie B, Woods JJ (1984) Changes in muscle contractile properties and neural control during human muscular fatigue. Muscle Nerve 7(9):691–699. https://doi.org/10.1002/mus.880070902
doi: 10.1002/mus.880070902
pubmed: 6100456
Blair SN, Haskell WL, Ho P, Paffenbarger RS Jr, Vranizan KM, Farquhar JW, Wood PD (1985) Assessment of habitual physical activity by a seven-day recall in a community survey and controlled experiments. Am J Epidemiol 122(5):794–804. https://doi.org/10.1093/oxfordjournals.aje.a114163
doi: 10.1093/oxfordjournals.aje.a114163
pubmed: 3876763
Buckthorpe M, Roi GS (2017) The time has come to incorporate a greater focus on rate of force development training in the sports injury rehabilitation process. Muscles Ligaments Tendons J 7(3):435–441
doi: 10.11138/mltj/2017.7.3.435
pubmed: 29387636
Burke D (2002) Effects of activity on axonal excitability: implications for motor control studies. Adv Exp Med Biol 508:33–37. https://doi.org/10.1007/978-1-4615-0713-0_5
doi: 10.1007/978-1-4615-0713-0_5
pubmed: 12171128
Charlson ME, Pompei P, Ales KL, MacKenzie CR (1987) A new method of classifying prognostic comorbidity in longitudinal studies: development and validation. J Chronic Dis 40(5):373–383. https://doi.org/10.1016/0021-9681(87)90171-8
doi: 10.1016/0021-9681(87)90171-8
pubmed: 3558716
Chatrenet A, Beaune B, Fois A, Pouliquen C, Audebrand JM, Torreggiani M, Piccoli GB (2020) Physiopathology of neuromuscular function related to fatigue in chronic renal disease in the elderly (PIONEER): study protocol. BMC Nephrol 21(1):305. https://doi.org/10.1186/s12882-020-01976-6
doi: 10.1186/s12882-020-01976-6
pubmed: 32711479
pmcid: 7382847
Chatrenet A, Piccoli G, Anthierens A, Torreggiani M, Audebrand JM, Morel B, Durand S (2023) Neural drive impairment in chronic kidney disease patients is associated with neuromuscular fatigability and fatigue. Med Sci Sports Exerc 55(4):727–739. https://doi.org/10.1249/mss.0000000000003090
doi: 10.1249/mss.0000000000003090
pubmed: 36508212
De Blasi RA, Luciani R, Punzo G, Arcioni R, Romano R, Boezi M, Menè P (2009) Microcirculatory changes and skeletal muscle oxygenation measured at rest by non-infrared spectroscopy in patients with and without diabetes undergoing haemodialysis. Crit Care 13(Suppl 5):S9. https://doi.org/10.1186/cc8007
doi: 10.1186/cc8007
pubmed: 19951393
pmcid: 2786111
Downey RM, Liao P, Millson EC, Quyyumi AA, Sher S, Park J (2017) Endothelial dysfunction correlates with exaggerated exercise pressor response during whole body maximal exercise in chronic kidney disease. Am J Physiol Renal Physiol 312(5):F917-f924. https://doi.org/10.1152/ajprenal.00603.2016
doi: 10.1152/ajprenal.00603.2016
pubmed: 28274927
pmcid: 5451552
DuPont JJ, Ramick MG, Farquhar WB, Townsend RR, Edwards DG (2014) NADPH oxidase-derived reactive oxygen species contribute to impaired cutaneous microvascular function in chronic kidney disease. Am J Physiol Renal Physiol 306(12):F1499-1506. https://doi.org/10.1152/ajprenal.00058.2014
doi: 10.1152/ajprenal.00058.2014
pubmed: 24761000
pmcid: 4059972
Enoka RM, Stuart DG (1992) Neurobiology of muscle fatigue. J Appl Physiol 72(5):1631–1648. https://doi.org/10.1152/jappl.1992.72.5.1631
doi: 10.1152/jappl.1992.72.5.1631
pubmed: 1601767
Enoki Y, Watanabe H, Arake R, Fujimura R, Ishiodori K, Imafuku T, Maruyama T (2017) Potential therapeutic interventions for chronic kidney disease-associated sarcopenia via indoxyl sulfate-induced mitochondrial dysfunction. J Cachexia Sarcopenia Muscle 8(5):735–747. https://doi.org/10.1002/jcsm.12202
doi: 10.1002/jcsm.12202
pubmed: 28608457
pmcid: 5659061
Fahal IH, Bell GM, Bone JM, Edwards RH (1997) Physiological abnormalities of skeletal muscle in dialysis patients. Nephrol Dial Transplant 12(1):119–127. https://doi.org/10.1093/ndt/12.1.119
doi: 10.1093/ndt/12.1.119
pubmed: 9027785
Ferrari M, Muthalib M, Quaresima V (2011) The use of near-infrared spectroscopy in understanding skeletal muscle physiology: recent developments. Philos Trans A Math Phys Eng Sci 369(1955):4577–4590. https://doi.org/10.1098/rsta.2011.0230
doi: 10.1098/rsta.2011.0230
pubmed: 22006907
Fouque D, Kalantar-Zadeh K, Kopple J, Cano N, Chauveau P, Cuppari L, Wanner C (2008) A proposed nomenclature and diagnostic criteria for protein-energy wasting in acute and chronic kidney disease. Kidney Int 73(4):391–398. https://doi.org/10.1038/sj.ki.5002585
doi: 10.1038/sj.ki.5002585
pubmed: 18094682
Gamboa JL, Billings FTT, Bojanowski MT, Gilliam LA, Yu C, Roshanravan B, Brown NJ (2016) Mitochondrial dysfunction and oxidative stress in patients with chronic kidney disease. Physiol Rep. https://doi.org/10.14814/phy2.12780
doi: 10.14814/phy2.12780
pubmed: 27162261
pmcid: 4873632
Gamboa JL, Roshanravan B, Towse T, Keller CA, Falck AM, Yu C, Ikizler TA (2020) Skeletal is muscle mitochondrial dysfunction present in patients with CKD before initiation of maintenance hemodialysis. Clin J Am Soc Nephrol 15(7):926–936. https://doi.org/10.2215/cjn.10320819
doi: 10.2215/cjn.10320819
pubmed: 32591419
pmcid: 7341789
Glatter KA, Graves SW, Hollenberg NK, Soszynski PA, Tao QF, Frem GJ, Lazarus JM (1994) Sustained volume expansion and [Na, K]ATPase inhibition in chronic renal failure. Am J Hypertens 7(11):1016–1025. https://doi.org/10.1093/ajh/7.11.1016
doi: 10.1093/ajh/7.11.1016
pubmed: 7848616
Grassi B, Pogliaghi S, Rampichini S, Quaresima V, Ferrari M, Marconi C, Cerretelli P (2003) Muscle oxygenation and pulmonary gas exchange kinetics during cycling exercise on-transitions in humans. J Appl Physiol 95(1):149–158. https://doi.org/10.1152/japplphysiol.00695.2002
doi: 10.1152/japplphysiol.00695.2002
pubmed: 12611769
Gollie JM, Harris-Love MO, Patel SS, Shara NM, Blackman MR (2021) Rate of force development is related to maximal force and sit-to-stand performance in men with stages 3b and 4 chronic kidney disease. Front Rehabil Sci 2:734705
doi: 10.3389/fresc.2021.734705
pubmed: 34708217
pmcid: 8547335
Hepple RT (2002) The role of O
doi: 10.1139/h02-004
pubmed: 11880691
Hermens HJ, Freriks B, Disselhorst-Klug C, Rau G (2000) Development of recommendations for SEMG sensors and sensor placement procedures. J Electromyogr Kinesiol 10(5):361–374. https://doi.org/10.1016/s1050-6411(00)00027-4
doi: 10.1016/s1050-6411(00)00027-4
pubmed: 11018445
Johansen KL, Kaysen GA, Young BS, Hung AM, da Silva M, Chertow GM (2003) Longitudinal study of nutritional status, body composition, and physical function in hemodialysis patients. Am J Clin Nutr 77(4):842–846. https://doi.org/10.1093/ajcn/77.4.842
doi: 10.1093/ajcn/77.4.842
pubmed: 12663281
Johansen KL, Doyle J, Sakkas GK, Kent-Braun JA (2005) Neural and metabolic mechanisms of excessive muscle fatigue in maintenance hemodialysis patients. Am J Physiol Regul Integr Comp Physiol 289(3):R805-813. https://doi.org/10.1152/ajpregu.00187.2005
doi: 10.1152/ajpregu.00187.2005
pubmed: 15905222
Kanai H, Hirakata H, Nakane H, Fujii K, Hirakata E, Ibayashi S, Kuwabara Y (2001) Depressed cerebral oxygen metabolism in patients with chronic renal failure: a positron emission tomography study. Am J Kidney Dis 38(4 Suppl 1):S129-133. https://doi.org/10.1053/ajkd.2001.27421
doi: 10.1053/ajkd.2001.27421
pubmed: 11576938
Kestenbaum B, Gamboa J, Liu S, Ali AS, Shankland E, Jue T, Roshanravan B (2020) Impaired skeletal muscle mitochondrial bioenergetics and physical performance in chronic kidney disease. JCI Insight. https://doi.org/10.1172/jci.insight.133289
doi: 10.1172/jci.insight.133289
pubmed: 32161192
pmcid: 7141399
Kirkman DL, Muth BJ, Ramick MG, Townsend RR, Edwards DG (2018) Role of mitochondria-derived reactive oxygen species in microvascular dysfunction in chronic kidney disease. Am J Physiol Renal Physiol 314(3):F423-f429. https://doi.org/10.1152/ajprenal.00321.2017
doi: 10.1152/ajprenal.00321.2017
pubmed: 29117995
Kluger BM, Krupp LB, Enoka RM (2013) Fatigue and fatigability in neurologic illnesses: proposal for a unified taxonomy. Neurology 80(4):409–416. https://doi.org/10.1212/WNL.0b013e31827f07be
doi: 10.1212/WNL.0b013e31827f07be
pubmed: 23339207
pmcid: 3589241
Kovarova L, Valerianova A, Kmentova T, Lachmanova J, Hladinova Z, Malik J (2018) Low cerebral oxygenation is associated with cognitive impairment in chronic hemodialysis patients. Nephron 139(2):113–119. https://doi.org/10.1159/000487092
doi: 10.1159/000487092
pubmed: 29439251
Krupp LB, Serafin DJ, Christodoulou C (2010) Multiple sclerosis-associated fatigue. Expert Rev Neurother 10(9):1437–1447. https://doi.org/10.1586/ern.10.99
doi: 10.1586/ern.10.99
pubmed: 20819014
Lännergren J, Westerblad H (1991) Force decline due to fatigue and intracellular acidification in isolated fibres from mouse skeletal muscle. J Physiol 434:307–322. https://doi.org/10.1113/jphysiol.1991.sp018471
doi: 10.1113/jphysiol.1991.sp018471
pubmed: 1902515
pmcid: 1181419
Levey AS, Eckardt KU, Dorman NM, Christiansen SL, Hoorn EJ, Ingelfinger JR, Winkelmayer WC (2020) Nomenclature for kidney function and disease: report of a Kidney Disease: Improving Global Outcomes (KDIGO) Consensus Conference. Kidney Int 97(6):1117–1129. https://doi.org/10.1016/j.kint.2020.02.010
doi: 10.1016/j.kint.2020.02.010
pubmed: 32409237
Macdonald JH, Fearn L, Jibani M, Marcora SM (2012) Exertional fatigue in patients with CKD. Am J Kidney Dis 60(6):930–939. https://doi.org/10.1053/j.ajkd.2012.06.021
doi: 10.1053/j.ajkd.2012.06.021
pubmed: 22883133
Marrades RM, Roca J, Campistol JM, Diaz O, Barberá JA, Torregrosa JV, Wagner PD (1996) Effects of erythropoietin on muscle O2 transport during exercise in patients with chronic renal failure. J Clin Invest 97(9):2092–2100. https://doi.org/10.1172/jci118646
doi: 10.1172/jci118646
pubmed: 8621799
pmcid: 507284
McGuire S, Horton EJ, Renshaw D, Chan K, Krishnan N, McGregor G (2020) Ventilatory and chronotropic incompetence during incremental and constant load exercise in end-stage renal disease: a comparative physiology study. Am J Physiol Renal Physiol 319(3):F515-f522. https://doi.org/10.1152/ajprenal.00258.2020
doi: 10.1152/ajprenal.00258.2020
pubmed: 32744086
pmcid: 7509284
Merton PA (1954) Voluntary strength and fatigue. J Physiol 123:553–164
doi: 10.1113/jphysiol.1954.sp005070
pubmed: 13152698
pmcid: 1366225
Miró O, Marrades RM, Roca J, Sala E, Masanés F, Campistol JM, Cardellach F (2002) Skeletal muscle mitochondrial function is preserved in young patients with chronic renal failure. Am J Kidney Dis 39(5):1025–1031. https://doi.org/10.1053/ajkd.2002.32776
doi: 10.1053/ajkd.2002.32776
pubmed: 11979346
Moore GE, Bertocci LA, Painter PL (1993) 31P-magnetic resonance spectroscopy assessment of subnormal oxidative metabolism in skeletal muscle of renal failure patients. J Clin Invest 91(2):420–424. https://doi.org/10.1172/jci116217
doi: 10.1172/jci116217
pubmed: 8432850
pmcid: 287944
Müntener M, Käser L, Weber J, Berchtold MW (1995) Increase of skeletal muscle relaxation speed by direct injection of parvalbumin cDNA. Proc Natl Acad Sci USA 92(14):6504–6508. https://doi.org/10.1073/pnas.92.14.6504
doi: 10.1073/pnas.92.14.6504
pubmed: 7604022
pmcid: 41546
Murtagh FE, Addington-Hall J, Higginson IJ (2007) The prevalence of symptoms in end-stage renal disease: a systematic review. Adv Chronic Kidney Dis 14(1):82–99. https://doi.org/10.1053/j.ackd.2006.10.001
doi: 10.1053/j.ackd.2006.10.001
pubmed: 17200048
Nielsen HB, Boesen M, Secher NH (2001) Near-infrared spectroscopy determined brain and muscle oxygenation during exercise with normal and resistive breathing. Acta Physiol Scand 171(1):63–70. https://doi.org/10.1046/j.1365-201X.2001.00782.x
doi: 10.1046/j.1365-201X.2001.00782.x
pubmed: 11350264
Nishikawa M, Ishimori N, Takada S, Saito A, Kadoguchi T, Furihata T, Tsutsui H (2015) AST-120 ameliorates lowered exercise capacity and mitochondrial biogenesis in the skeletal muscle from mice with chronic kidney disease via reducing oxidative stress. Nephrol Dial Transplant 30(6):934–942. https://doi.org/10.1093/ndt/gfv103
doi: 10.1093/ndt/gfv103
pubmed: 25878055
Nybo L, Rasmussen P (2007) Inadequate cerebral oxygen delivery and central fatigue during strenuous exercise. Exerc Sport Sci Rev 35(3):110–118. https://doi.org/10.1097/jes.0b013e3180a031ec
doi: 10.1097/jes.0b013e3180a031ec
pubmed: 17620929
Passauer J, Pistrosch F, Büssemaker E, Lässig G, Herbrig K, Gross P (2005) Reduced agonist-induced endothelium-dependent vasodilation in uremia is attributable to an impairment of vascular nitric oxide. J Am Soc Nephrol 16(4):959–965. https://doi.org/10.1681/asn.2004070582
doi: 10.1681/asn.2004070582
pubmed: 15728785
Price SR, Gooch JL, Donaldson SK, Roberts-Wilson TK (2010) Muscle atrophy in chronic kidney disease results from abnormalities in insulin signaling. J Ren Nutr 20(5 Suppl):S24-28. https://doi.org/10.1053/j.jrn.2010.05.007
doi: 10.1053/j.jrn.2010.05.007
pubmed: 20797566
pmcid: 2937009
Prinsen H, van Dijk JP, Zwarts MJ, Leer JW, Bleijenberg G, van Laarhoven HW (2015) The role of central and peripheral muscle fatigue in postcancer fatigue: a randomized controlled trial. J Pain Symptom Manage 49(2):173–182. https://doi.org/10.1016/j.jpainsymman.2014.06.020
doi: 10.1016/j.jpainsymman.2014.06.020
pubmed: 25150812
Rossman MJ, Venturelli M, McDaniel J, Amann M, Richardson RS (2012) Muscle mass and peripheral fatigue: a potential role for afferent feedback? Acta Physiol (oxf) 206(4):242–250. https://doi.org/10.1111/j.1748-1716.2012.02471.x
doi: 10.1111/j.1748-1716.2012.02471.x
pubmed: 22762286
Roumeliotis S, Mallamaci F, Zoccali C (2020) Endothelial dysfunction in chronic kidney disease, from biology to clinical outcomes: a 2020 update. J Clin Med. https://doi.org/10.3390/jcm9082359
doi: 10.3390/jcm9082359
pubmed: 32718053
pmcid: 7465707
Sangkabutra T, Crankshaw DP, Schneider C, Fraser SF, Sostaric S, Mason K, McKenna MJ (2003) Impaired K+ regulation contributes to exercise limitation in end-stage renal failure. Kidney Int 63(1):283–290. https://doi.org/10.1046/j.1523-1755.2003.00739.x
doi: 10.1046/j.1523-1755.2003.00739.x
pubmed: 12472794
Sawant A, Garland SJ, House AA, Overend TJ (2011) Morphological, electrophysiological, and metabolic characteristics of skeletal muscle in people with end-stage renal disease: a critical review. Physiother Can 63(3):355–376. https://doi.org/10.3138/ptc.2010-18
doi: 10.3138/ptc.2010-18
pubmed: 22654242
pmcid: 3157996
Segura-Ortí E, Gordon PL, Doyle JW, Johansen KL (2018) Correlates of physical functioning and performance across the spectrum of kidney function. Clin Nurs Res 27(5):579–596. https://doi.org/10.1177/1054773816689282
doi: 10.1177/1054773816689282
pubmed: 28114792
Singh R, Kluding PM (2013) Fatigue and related factors in people with type 2 diabetes. Diabetes Educ 39(3):320–326. https://doi.org/10.1177/0145721713479144
doi: 10.1177/0145721713479144
pubmed: 23475184
Slee AD (2012) Exploring metabolic dysfunction in chronic kidney disease. Nutr Metab (lond) 9(1):36. https://doi.org/10.1186/1743-7075-9-36
doi: 10.1186/1743-7075-9-36
pubmed: 22537670
Slessarev M, Mahmoud O, Albakr R, Dorie J, Tamasi T, McIntyre CW (2021) Hemodialysis patients have impaired cerebrovascular reactivity to CO(2) compared to chronic kidney disease patients and healthy controls: a pilot study. Kidney Int Rep 6(7):1868–1877. https://doi.org/10.1016/j.ekir.2021.04.005
doi: 10.1016/j.ekir.2021.04.005
pubmed: 34307981
pmcid: 8258459
Stenvinkel P, Carrero JJ, von Walden F, Ikizler TA, Nader GA (2016) Muscle wasting in end-stage renal disease promulgates premature death: established, emerging and potential novel treatment strategies. Nephrol Dial Transplant 31(7):1070–1077. https://doi.org/10.1093/ndt/gfv122
doi: 10.1093/ndt/gfv122
pubmed: 25910496
Stokes GS, Norris LA, Marwood JF, Monaghan JC, Caterson RJ (1988) An Na+-K+-ATPase inhibitor which circulates in renal failure but not in essential hypertension. Prog Biochem Pharmacol 23:46–54
pubmed: 2847190
Szubski C, Burtscher M, Löscher WN (2007) Neuromuscular fatigue during sustained contractions performed in short-term hypoxia. Med Sci Sports Exerc 39(6):948–954. https://doi.org/10.1249/mss.0b013e3180479918
doi: 10.1249/mss.0b013e3180479918
pubmed: 17545884
Taylor JL, Gandevia SC (2008) A comparison of central aspects of fatigue in submaximal and maximal voluntary contractions. J Appl Physiol 104(2):542–550. https://doi.org/10.1152/japplphysiol.01053.2007
doi: 10.1152/japplphysiol.01053.2007
pubmed: 18032577
Thomas K, Elmeua M, Howatson G, Goodall S (2016) Intensity-dependent contribution of neuromuscular fatigue after constant-load cycling. Med Sci Sports Exerc 48(9):1751–1760. https://doi.org/10.1249/mss.0000000000000950
doi: 10.1249/mss.0000000000000950
pubmed: 27187101
Twomey R, Aboodarda SJ, Kruger R, Culos-Reed SN, Temesi J, Millet GY (2017) Neuromuscular fatigue during exercise: Methodological considerations, etiology and potential role in chronic fatigue. Neurophysiol Clin 47(2):95–110. https://doi.org/10.1016/j.neucli.2017.03.002
doi: 10.1016/j.neucli.2017.03.002
pubmed: 28434551
Verges S, Sager Y, Erni C, Spengler CM (2007) Expiratory muscle fatigue impairs exercise performance. Eur J Appl Physiol 101(2):225–232. https://doi.org/10.1007/s00421-007-0491-y
doi: 10.1007/s00421-007-0491-y
pubmed: 17546459
Verges S, Rupp T, Jubeau M, Wuyam B, Esteve F, Levy P, Millet GY (2012) Cerebral perturbations during exercise in hypoxia. Am J Physiol Regul Integr Comp Physiol 302(8):R903-916. https://doi.org/10.1152/ajpregu.00555.2011
doi: 10.1152/ajpregu.00555.2011
pubmed: 22319046
Wallin H, Asp AM, Wallquist C, Jansson E, Caidahl K, Hylander Rössner B, Eriksson MJ (2018) Gradual reduction in exercise capacity in chronic kidney disease is associated with systemic oxygen delivery factors. PLoS ONE 13(12):e0209325. https://doi.org/10.1371/journal.pone.0209325
doi: 10.1371/journal.pone.0209325
pubmed: 30566512
pmcid: 6300328
Zhou Y, Hellberg M, Svensson P, Höglund P, Clyne N (2018) Sarcopenia and relationships between muscle mass, measured glomerular filtration rate and physical function in patients with chronic kidney disease stages 3–5. Nephrol Dial Transplant 33(2):342–348. https://doi.org/10.1093/ndt/gfw466
doi: 10.1093/ndt/gfw466
pubmed: 28340152