Abstract
Purpose
It was hypothesized that patients with chronic obstructive pulmonary disease (COPD) would exhibit a slow muscle deoxygenation (HHb) recovery time when compared with sedentary controls.
Methods
Neuromuscular electrical stimulation (NMES 40 and 50 mA, 50 Hz, 400 µs) was employed to induce isometric contraction of the quadriceps. Microvascular oxygen extraction (µO2EF) and HHb were estimated by near-infrared spectroscopy (NIRS). Recovery kinetic was characterized by measuring the time constant Tau (HHb-τ). Torque and work were measured by isokinetic dynamometry in 13 non-hypoxaemic patients with moderate-to-severe COPD [SpO2 = 94.1 ± 1.6 %; FEV1 (% predict) 48.0 ± 9.6; GOLD II–III] and 13 age- and sex-matched sedentary controls.
Results
There was no desaturation in either group during NMES. Torque and work were reduced in COPD versus control for 40 and 50 mA [torque (Nm) 50 mA = 28.9 ± 6.9 vs 46.1 ± 14.2; work (J) 50 mA = 437.2 ± 130.0 vs. 608.3 ± 136.8; P < 0.05 for all]. High µO2EF values were observed in the COPD group at both NMES intensities (corrected by muscle mass 50 mA = 6.18 ± 1.1 vs. 4.68 ± 1.0 %/kg; corrected by work 50 mA = 0.12 ± 0.05 vs. 0.07 ± 0.02 %/J; P < 0.05 for all). Absolute values of HHb-τ (50 mA = 31.11 ± 9.27 vs. 18.08 ± 10.70 s), corrected for muscle mass (50 mA 3.80 ± 1.28 vs. 2.05 ± 1.45 s/kg) and corrected for work (50 mA = 0.08 ± 0.04 vs. 0.03 ± 0.02 s/J) were reduced in COPD (P < 0.05 for all). The variables behaviour for 40 mA was similar to those of 50 mA.
Conclusions
COPD patients exhibited a slower muscle deoxygenation recovery time after NMES. The absence of desaturation, low torque and work, high µO2EF and high values for recovery time corrected by muscle mass and work suggest that intrinsic muscle dysfunction has an impact on muscle recovery capacity.
Similar content being viewed by others
Abbreviations
- ADP:
-
Adenosine diphosphate
- CaO2 :
-
Arterial blood oxygen content
- COPD :
-
Chronic obstructive pulmonary disease
- DEXA:
-
Dual energy X-ray absorptiometry
- EMG:
-
Electromyography
- FAD:
-
Flavin adenine dinucleotide
- FFM:
-
Fat-free mass
- HHb:
-
Deoxygenated haemoglobin/myoglobin
- µO2EF:
-
Microvascular oxygen extraction fraction
- NIRS:
-
Near-infrared spectroscopy
- NMES:
-
Neuromuscular electrical stimulation
- NAD:
-
Nicotinamide adenine dinucleotide
- O2Hb:
-
Oxygenated haemoglobin/myoglobin
- PCr:
-
Phosphocreatine
- Qt:
-
Cardiac output
- SmO2 :
-
Muscle saturation
- SpO2:
-
Arterial blood oxygen saturation
- tHb:
-
Total haemoglobin or blood volume
- TM:
-
Total mass
- τ:
-
Tau
- 31P-MRS:
-
31P-magnetic resonance spectroscopy
References
Adami A, Koga S, Kondo N, Cannon DT, Kowalchuk JM, Amano T, Rossiter HB (2015) Changes in whole tissue heme concentration dissociates muscle deoxygenation from muscle oxygen extraction during passive head-up tilt. J Appl Physiol 118(9):1091–1099. doi:10.1152/japplphysiol.00918.2014
Ambrosino N, Strambi S (2004) New strategies to improve exercise tolerance in chronic obstructive pulmonary disease. Eur Respir J 24(2):313–322
Berton DC, Barbosa PB, Takara LS, Chiappa GR, Siqueira AC, Bravo DM, Ferreira LF, Neder JA (2010) Bronchodilators accelerate the dynamics of muscle O2 delivery and utilisation during exercise in COPD. Thorax 65(7):588–593. doi:10.1136/thx.2009.120857
Bickel CS, Gregory CM, Dean JC (2011) Motor unit recruitment during neuromuscular electrical stimulation: a critical appraisal. Eur J Appl Physiol 111(10):2399–2407. doi:10.1007/s00421-011-2128-4
Billaut F, Buchheit M (2013) Repeated-sprint performance and vastus lateralis oxygenation: effect of limited O(2) availability. Scand J Med Sci Sports 23(3):e185–e193. doi:10.1111/sms.12052
Borghi-Silva A, Oliveira CC, Carrascosa C, Maia J, Berton DC, Queiroga F Jr, Ferreira EM, Almeida DR, Nery LE, Neder JA (2008) Respiratory muscle unloading improves leg muscle oxygenation during exercise in patients with COPD. Thorax 63(10):910–915
Bourjeily-Habr G, Rochester CL, Palermo F, Snyder P, Mohsenin V (2002) Randomised controlled trial of transcutaneous electrical muscle stimulation of the lower extremities in patients with chronic obstructive pulmonary disease. Thorax 57(12):1045–1049
Chiappa GR, Borghi-Silva A, Ferreira LF, Carrascosa C, Oliveira CC, Maia J, Gimenes AC, Queiroga F Jr, Berton D, Ferreira EM, Nery LE, Neder JA (2008) Kinetics of muscle deoxygenation are accelerated at the onset of heavy-intensity exercise in patients with COPD: relationship to central cardiovascular dynamics. J Appl Physiol 104(5):1341–1350
Chiappa GR, Queiroga F Jr, Meda E, Ferreira LF, Diefenthaeler F, Nunes M, Vaz MA, Machado MC, Nery LE, Neder JA (2009) Heliox improves oxygen delivery and utilization during dynamic exercise in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 179(11):1004–1010
Chibalin AV, Heiny JA, Benziane B, Prokofiev AV, Vasiliev AV, Kravtsova VV, Krivoi II (2012) Chronic nicotine modifies skeletal muscle Na, K-ATPase activity through its interaction with the nicotinic acetylcholine receptor and phospholemman. PLoS One 7(3):e33719. doi:10.1371/journal.pone.0033719
Clarenbach CF, Senn O, Sievi NA, Camen G, van Gestel AJ, Rossi VA, Puhan MA, Thurnheer R, Russi EW, Kohler M (2013) Determinants of endothelial function in patients with COPD. Eur Respir J 42(5):1194–1204. doi:10.1183/09031936.00144612
Conley KE, Amara CE, Jubrias SA, Marcinek DJ (2007) Mitochondrial function, fibre types and ageing: new insights from human muscle in vivo. Exp Physiol 92(2):333–339. doi:10.1113/expphysiol.2006.034330
Dal Corso S, Napolis L, Malaguti C, Gimenes AC, Albuquerque A, Nogueira CR, De Fuccio MB, Pereira RD, Bulle A, McFarlane N, Nery LE, Neder JA (2007) Skeletal muscle structure and function in response to electrical stimulation in moderately impaired COPD patients. Respir Med 101(6):1236–1243
Fabbri LM, Hurd SS, Committee GS (2003) Global strategy for the diagnosis, management and prevention of COPD: 2003 update. Eur Respir J 22(1):1–2
Gagnon P, Lemire BB, Dube A, Saey D, Porlier A, Croteau M, Provencher S, Debigare R, Maltais F (2014) Preserved function and reduced angiogenesis potential of the quadriceps in patients with mild COPD. Respir Res 15:4. doi:10.1186/1465-9921-15-4
Gifford JR, Trinity JD, Layec G, Garten RS, Park SY, Rossman MJ, Larsen S, Dela F, Richardson RS (2015) Quadriceps exercise intolerance in patients with chronic obstructive pulmonary disease: the potential role of altered skeletal muscle mitochondrial respiration. J Appl Physiol 119(8):882–888. doi:10.1152/japplphysiol.00460.2015
Glaister M (2005) Multiple sprint work: physiological responses, mechanisms of fatigue and the influence of aerobic fitness. Sports Med 35(9):757–777
Gosker HR, Wouters EF, van der Vusse GJ, Schols AM (2000) Skeletal muscle dysfunction in chronic obstructive pulmonary disease and chronic heart failure: underlying mechanisms and therapy perspectives. Am J Clin Nutr 71(5):1033–1047
Gosker HR, Zeegers MP, Wouters EF, Schols AM (2007) Muscle fibre type shifting in the vastus lateralis of patients with COPD is associated with disease severity: a systematic review and meta-analysis. Thorax 62(11):944–949. doi:10.1136/thx.2007.078980
Green H, MacDougall J, Tarnopolsky M, Melissa NL (1999) Downregulation of Na+–K+-ATPase pumps in skeletal muscle with training in normobaric hypoxia. J Appl Physiol 86(5):1745–1748
Green H, Roy B, Grant S, Burnett M, Tupling R, Otto C, Pipe A, McKenzie D (2000) Downregulation in muscle Na(+)–K(+)-ATPase following a 21-day expedition to 6,194 m. J Appl Physiol 88(2):634–640
Green HJ, Burnett ME, D’Arsigny CL, Webb KA, McBride I, Ouyang J, O’Donnell DE (2009) Vastus lateralis Na(+)–K(+)-ATPase activity, protein, and isoform distribution in chronic obstructive pulmonary disease. Muscle Nerve 40(1):62–68. doi:10.1002/mus.21296
Haseler LJ, Hogan MC, Richardson RS (1999) Skeletal muscle phosphocreatine recovery in exercise-trained humans is dependent on O2 availability. J Appl Physiol 86(6):2013–2018
Hennings K, Arendt-Nielsen L, Andersen OK (2005) Breakdown of accommodation in nerve: a possible role for persistent sodium current. Theor Biol Med Model 2:16. doi:10.1186/1742-4682-2-16
Karatzaferi C, de Haan A, Ferguson RA, van Mechelen W, Sargeant AJ (2001) Phosphocreatine and ATP content in human single muscle fibres before and after maximum dynamic exercise. Pflugers Arch 442(3):467–474
Karoli NA, Rebrov AP, Iudakova IuN (2004) Vascular endothelial dysfunction in patients with chronic obstructive lung diseases. Probl Tuberk Bolezn Legk 4:19–23
Kemp GJ, Taylor DJ, Radda GK (1993) Control of phosphocreatine resynthesis during recovery from exercise in human skeletal muscle. NMR Biomed 6(1):66–72
Kemps HM, Prompers JJ, Wessels B, De Vries WR, Zonderland ML, Thijssen EJ, Nicolay K, Schep G, Doevendans PA (2010) Skeletal muscle metabolic recovery following submaximal exercise in chronic heart failure is limited more by O(2) delivery than O(2) utilization. Clin Sci (Lond) 118(3):203–210
Koga S, Rossiter HB, Heinonen I, Musch TI, Poole DC (2014) Dynamic heterogeneity of exercising muscle blood flow and O2 utilization. Med Sci Sports Exerc 46(5):860–876. doi:10.1249/MSS.0000000000000178
Koga S, Barstow TJ, Okushima D, Rossiter HB, Kondo N, Ohmae E, Poole DC (2015) Validation of a high-power, time-resolved, near-infrared spectroscopy system for measurement of superficial and deep muscle deoxygenation during exercise. J Appl Physiol 118(11):1435–1442. doi:10.1152/japplphysiol.01003.2014
Konokhova Y, Spendiff S, Jagoe RT, Aare S, Kapchinsky S, MacMillan NJ, Rozakis P, Picard M, Aubertin-Leheudre M, Pion CH, Bourbeau J, Hepple RT, Taivassalo T (2016) Failed upregulation of TFAM protein and mitochondrial DNA in oxidatively deficient fibers of chronic obstructive pulmonary disease locomotor muscle. Skelet Muscle 6:10. doi:10.1186/s13395-016-0083-9
Kutsuzawa T, Shioya S, Kurita D, Haida M, Ohta Y, Yamabayashi H (1992) 31P-NMR study of skeletal muscle metabolism in patients with chronic respiratory impairment. Am Rev Respir Dis 146(4):1019–1024. doi:10.1164/ajrccm/146.4.1019
Kutsuzawa T, Shioya S, Kurita D, Haida M, Ohta Y, Yamabayashi H (1995) Muscle energy metabolism and nutritional status in patients with chronic obstructive pulmonary disease. A 31P magnetic resonance study. Am J Respir Crit Care Med 152(2):647–652. doi:10.1164/ajrccm.152.2.7633721
Layec G, Haseler LJ, Hoff J, Richardson RS (2011) Evidence that a higher ATP cost of muscular contraction contributes to the lower mechanical efficiency associated with COPD: preliminary findings. Am J Physiol Regul Integr Comp Physiol 300(5):R1142–R1147. doi:10.1152/ajpregu.00835.2010
Maltais F, Decramer M, Casaburi R, Barreiro E, Burelle Y, Debigare R, Dekhuijzen PN, Franssen F, Gayan-Ramirez G, Gea J, Gosker HR, Gosselink R, Hayot M, Hussain SN, Janssens W, Polkey MI, Roca J, Saey D, Schols AM, Spruit MA, Steiner M, Taivassalo T, Troosters T, Vogiatzis I, Wagner PD, COPD AEAHCoLMDi (2014) An official American Thoracic Society/European Respiratory Society statement: update on limb muscle dysfunction in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 189(9):e15–e62. doi:10.1164/rccm.201402-0373ST
McCully KK, Iotti S, Kendrick K, Wang Z, Posner JD, Leigh J Jr, Chance B (1994) Simultaneous in vivo measurements of HbO2 saturation and PCr kinetics after exercise in normal humans. J Appl Physiol 77(1):5–10
McMahon S, Jenkins D (2002) Factors affecting the rate of phosphocreatine resynthesis following intense exercise. Sports Med 32(12):761–784
Medeiros WM, Fernandes MC, Azevedo DP, de Freitas FF, Amorim BC, Chiavegato LD, Hirai DM, O’Donnell DE, Neder JA (2015) Oxygen delivery-utilization mismatch in contracting locomotor muscle in COPD: peripheral factors. Am J Physiol Regul Integr Comp Physiol 308(2):R105–R111. doi:10.1152/ajpregu.00404.2014
Miller A, Strauss BJ, Mol S, Kyoong A, Holmes PH, Finlay P, Bardin PG, Guy P (2009) Dual-energy X-ray absorptiometry is the method of choice to assess body composition in COPD. Respirology 14(3):411–418
Neder JA (2008) The major limitation to exercise performance in COPD is inadequate energy supply to the respiratory and locomotor muscles vs. lower limb muscle dysfunction vs. dynamic hyperinflation. Interpretation of exercise intolerance in COPD requires an integrated, multisystemic approach. J Appl Physiol 105(2):758–759
Neder JA, Sword D, Ward SA, Mackay E, Cochrane LM, Clark CJ (2002) Home based neuromuscular electrical stimulation as a new rehabilitative strategy for severely disabled patients with chronic obstructive pulmonary disease (COPD). Thorax 57(4):333–337
Okamoto T, Kanazawa H, Hirata K, Yoshikawa J (2003) Evaluation of oxygen uptake kinetics and oxygen kinetics of peripheral skeletal muscle during recovery from exercise in patients with chronic obstructive pulmonary disease. Clin Physiol Funct Imaging 23(5):257–262
Pereira AC, Neder JA (2002) Diretrizes para Testes de Função Pulmonar. Braz J Pulmonol 28 (Suppl 3):1–221
Puente-Maestu L, Tena T, Trascasa C, Perez-Parra J, Godoy R, Garcia MJ, Stringer WW (2003) Training improves muscle oxidative capacity and oxygenation recovery kinetics in patients with chronic obstructive pulmonary disease. Eur J Appl Physiol 88(6):580–587. doi:10.1007/s00421-002-0743-9
Puente-Maestu L, Perez-Parra J, Godoy R, Moreno N, Tejedor A, Gonzalez-Aragoneses F, Bravo JL, Alvarez FV, Camano S, Agusti A (2009) Abnormal mitochondrial function in locomotor and respiratory muscles of COPD patients. Eur Respir J 33(5):1045–1052. doi:10.1183/09031936.00112408
Quaresima V, Ferrari M (2009) Muscle oxygenation by near-infrared-based tissue oximeters. J Appl Physiol 107(1):371. doi:10.1152/japplphysiol.00215.2009 (Author reply 372–373)
Quaresima V, Lepanto R, Ferrari M (2003) The use of near infrared spectroscopy in sports medicine. J Sports Med Phys Fitness 43(1):1–13
Richardson RS, Grassi B, Gavin TP, Haseler LJ, Tagore K, Roca J, Wagner PD (1999) Evidence of O2 supply-dependent VO2 max in the exercise-trained human quadriceps. J Appl Physiol 86(3):1048–1053
Richardson RS, Leek BT, Gavin TP, Haseler LJ, Mudaliar SR, Henry R, Mathieu-Costello O, Wagner PD (2004) Reduced mechanical efficiency in chronic obstructive pulmonary disease but normal peak VO2 with small muscle mass exercise. Am J Respir Crit Care Med 169(1):89–96. doi:10.1164/rccm.200305-627OC
Rossiter HB, Ward SA, Howe FA, Kowalchuk JM, Griffiths JR, Whipp BJ (2002) Dynamics of intramuscular 31P-MRS P(i) peak splitting and the slow components of PCr and O2 uptake during exercise. J Appl Physiol 93(6):2059–2069. doi:10.1152/japplphysiol.00446.2002
Ryan TE, Southern WM, Reynolds MA, McCully KK (2013) A cross-validation of near-infrared spectroscopy measurements of skeletal muscle oxidative capacity with phosphorus magnetic resonance spectroscopy. J Appl Physiol 115(12):1757–1766. doi:10.1152/japplphysiol.00835.2013
Sillen MJ, Janssen PP, Akkermans MA, Wouters EF, Spruit MA (2008) The metabolic response during resistance training and neuromuscular electrical stimulation (NMES) in patients with COPD, a pilot study. Respir Med 102(5):786–789
Sillen MJ, Franssen FM, Vaes AW, Delbressine JM, Wouters EF, Spruit MA (2014) Metabolic load during strength training or NMES in individuals with COPD: results from the DICES trial. BMC Pulm Med 14:146. doi:10.1186/1471-2466-14-146
Southern WM, Ryan TE, Reynolds MA, McCully K (2014) Reproducibility of near-infrared spectroscopy measurements of oxidative function and postexercise recovery kinetics in the medial gastrocnemius muscle. Appl Physiol Nutr Metabol (Physiol Appl Nutr Metab) 39(5):521–529. doi:10.1139/apnm-2013-0347
Tada H, Kato H, Misawa T, Sasaki F, Hayashi S, Takahashi H, Kutsumi Y, Ishizaki T, Nakai T, Miyabo S (1992) 31P-nuclear magnetic resonance evidence of abnormal skeletal muscle metabolism in patients with chronic lung disease and congestive heart failure. Eur Respir J 5(2):163–169
Taivassalo T, Hussain SN (2015) Contribution of the mitochondria to locomotor muscle dysfunction in COPD patients. Chest. doi:10.1016/j.chest.2015.11.021
Tanrikulu AC, Abakay A, Evliyaoglu O, Palanci Y (2011) Coenzyme Q10, copper, zinc, and lipid peroxidation levels in serum of patients with chronic obstructive pulmonary disease. Biol Trace Elem Res 143(2):659–667. doi:10.1007/s12011-010-8897-5
Valenza MC, Torres-Sanchez I, Cabrera-Martos I, Rodriguez-Torres J, Gonzalez-Jimenez E, Munoz-Casaubon T (2016) Physical activity as a predictor of absence of frailty in subjects with stable COPD and COPD exacerbation. Respir Care 61(2):212–219. doi:10.4187/respcare.04118
Vanderthommen M, Duteil S, Wary C, Raynaud JS, Leroy-Willig A, Crielaard JM, Carlier PG (2003) A comparison of voluntary and electrically induced contractions by interleaved 1H- and 31P-NMRS in humans. J Appl Physiol 94(3):1012–1024. doi:10.1152/japplphysiol.00887.2001
Vanhee JL, Voisin P, Vezirian T, Vanvelcenaher J (1996) Isokinetic trunk flexors and extensors performance with and without gravity correction. Isokinet Exerc Sci 6(2):89–94
Vivodtzev I, Pepin JL, Vottero G, Mayer V, Porsin B, Levy P, Wuyam B (2006) Improvement in quadriceps strength and dyspnea in daily tasks after 1 month of electrical stimulation in severely deconditioned and malnourished COPD. Chest 129(6):1540–1548. doi:10.1378/chest.129.6.1540
Vivodtzev I, Lacasse Y, Maltais F (2008) Neuromuscular electrical stimulation of the lower limbs in patients with chronic obstructive pulmonary disease. J Cardiopulm Rehabil Prevent 28(2):79–91. doi:10.1097/01.HCR.0000314201.02053.a3
Vivodtzev I, Debigare R, Gagnon P, Mainguy V, Saey D, Dube A, Pare ME, Belanger M, Maltais F (2012) Functional and muscular effects of neuromuscular electrical stimulation in patients with severe COPD: a randomized clinical trial. Chest 141(3):716–725. doi:10.1378/chest.11-0839
Wagner PD (2006) Skeletal muscles in chronic obstructive pulmonary disease: deconditioning, or myopathy? Respirology 11(6):681–686. doi:10.1111/j.1440-1843.2006.00939.x
Weindling AM (2010) Peripheral oxygenation and management in the perinatal period. Semin Fetal Neonatal Med 15(4):208–215. doi:10.1016/j.siny.2010.03.005
Westing SH, Seger JY (1989) Eccentric and concentric torque-velocity characteristics, torque output comparisons, and gravity effect torque corrections for the quadriceps and hamstring muscles in females. Int J Sports Med 10(3):175–180. doi:10.1055/s-2007-1024896
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
All authors have read and approved the manuscript. The authors declare no conflicts of interest.
Additional information
Communicated by David C. Poole.
Rights and permissions
About this article
Cite this article
Azevedo, D.d., Medeiros, W.M., de Freitas, F.F.M. et al. High oxygen extraction and slow recovery of muscle deoxygenation kinetics after neuromuscular electrical stimulation in COPD patients. Eur J Appl Physiol 116, 1899–1910 (2016). https://doi.org/10.1007/s00421-016-3442-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00421-016-3442-7