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Published in: Clinical and Experimental Nephrology 1/2019

Open Access 01-01-2019 | Original article

Characterising skeletal muscle haemoglobin saturation during exercise using near-infrared spectroscopy in chronic kidney disease

Authors: Thomas J. Wilkinson, Alice E. M. White, Daniel G. D. Nixon, Douglas W. Gould, Emma L. Watson, Alice C. Smith

Published in: Clinical and Experimental Nephrology | Issue 1/2019

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Abstract

Background

Chronic kidney disease (CKD) patients have reduced exercise capacity. Possible contributing factors may include impaired muscle O2 utilisation through reduced mitochondria number and/or function slowing the restoration of muscle ATP concentrations via oxidative phosphorylation. Using near-infrared spectroscopy (NIRS), we explored changes in skeletal muscle haemoglobin/myoglobin O2 saturation (SMO2%) during exercise.

Methods

24 CKD patients [58.3 (± 16.5) years, eGFR 56.4 (± 22.3) ml/min/1.73 m2] completed the incremental shuttle walk test (ISWT) as a marker of exercise capacity. Using NIRS, SMO2% was measured continuously before, during, and after (recovery) exercise. Exploratory differences were investigated between exercise capacity tertiles in CKD, and compared with six healthy controls.

Results

We identified two discrete phases; a decline in SMO2% during incremental exercise, followed by rapid increase upon cessation (recovery). Compared to patients with low exercise capacity [distance walked during ISWT, 269.0 (± 35.9) m], patients with a higher exercise capacity [727.1 (± 38.1) m] took 45% longer to reach their minimum SMO2% (P = .038) and recovered (half-time recovery) 79% faster (P = .046). Compared to controls, CKD patients took significantly 56% longer to recover (i.e., restore SMO2% to baseline, full recovery) (P = .014).

Conclusions

Using NIRS, we have determined for the first time in CKD, that favourable SMO2% kinetics (slower deoxygenation rate, quicker recovery) are associated with greater exercise capacity. These dysfunctional kinetics may indicate reduced mitochondria capacity to perform oxidative phosphorylation—a process essential for carrying out even simple activities of daily living. Accordingly, NIRS may provide a simple, low cost, and non-invasive means to evaluate muscle O2 kinetics in CKD.
Literature
1.
go back to reference Levey AS, Eckardt KU, Tsukamoto Y, et al. Definition and classification of chronic kidney disease: a position statement from Kidney Disease: Improving Global Outcomes (KDIGO). Kidney Int. 2005;67:2089–100.CrossRefPubMed Levey AS, Eckardt KU, Tsukamoto Y, et al. Definition and classification of chronic kidney disease: a position statement from Kidney Disease: Improving Global Outcomes (KDIGO). Kidney Int. 2005;67:2089–100.CrossRefPubMed
4.
go back to reference Zhou Y, Hellberg M, Svensson P, Höglund P, Clyne N. Sarcopenia and relationships between muscle mass, measured glomerular filtration rate and physical function in patients with chronic kidney disease stages 3–5. Nephrol Dial Transpl. 2017;33:342–8. https://doi.org/10.1093/ndt/gfw466.CrossRef Zhou Y, Hellberg M, Svensson P, Höglund P, Clyne N. Sarcopenia and relationships between muscle mass, measured glomerular filtration rate and physical function in patients with chronic kidney disease stages 3–5. Nephrol Dial Transpl. 2017;33:342–8. https://​doi.​org/​10.​1093/​ndt/​gfw466.CrossRef
10.
go back to reference Bassett DR Jr, Howley ET. Limiting factors for maximum oxygen uptake and determinants of endurance performance. Med Sci Sports Exerc. 2000;32:70–84.CrossRefPubMed Bassett DR Jr, Howley ET. Limiting factors for maximum oxygen uptake and determinants of endurance performance. Med Sci Sports Exerc. 2000;32:70–84.CrossRefPubMed
16.
go back to reference Yazdi PG, Moradi H, Yang JY, Wang PH, Vaziri ND. Skeletal muscle mitochondrial depletion and dysfunction in chronic kidney disease. Int J Clin Exp Med. 2013;6:532–9.PubMedPubMedCentral Yazdi PG, Moradi H, Yang JY, Wang PH, Vaziri ND. Skeletal muscle mitochondrial depletion and dysfunction in chronic kidney disease. Int J Clin Exp Med. 2013;6:532–9.PubMedPubMedCentral
18.
go back to reference Lim PS, Ma YS, Cheng YM, et al. Mitochondrial DNA mutations and oxidative damage in skeletal muscle of patients with chronic uremia. J Biomed Sci. 2002;9:549–60.CrossRefPubMed Lim PS, Ma YS, Cheng YM, et al. Mitochondrial DNA mutations and oxidative damage in skeletal muscle of patients with chronic uremia. J Biomed Sci. 2002;9:549–60.CrossRefPubMed
19.
go back to reference Kemp GJ, Radda GK. Quantitative interpretation of bioenergetic data from 31P and 1H magnetic resonance spectroscopic studies of skeletal muscle: an analytical review. Magn Reson Q. 1994;10:43–63.PubMed Kemp GJ, Radda GK. Quantitative interpretation of bioenergetic data from 31P and 1H magnetic resonance spectroscopic studies of skeletal muscle: an analytical review. Magn Reson Q. 1994;10:43–63.PubMed
20.
go back to reference Jones S, Chiesa ST, Chaturvedi N, Hughes AD. Recent developments in near-infrared spectroscopy (NIRS) for the assessment of local skeletal muscle microvascular function and capacity to utilise oxygen. Artery Res. 2016;16:25–33.CrossRefPubMedPubMedCentral Jones S, Chiesa ST, Chaturvedi N, Hughes AD. Recent developments in near-infrared spectroscopy (NIRS) for the assessment of local skeletal muscle microvascular function and capacity to utilise oxygen. Artery Res. 2016;16:25–33.CrossRefPubMedPubMedCentral
22.
go back to reference Bauer TA, Brass EP, Hiatt WR. Impaired muscle oxygen use at onset of exercise in peripheral arterial disease. J Vasc Surg. 2004;40:488–93.CrossRefPubMed Bauer TA, Brass EP, Hiatt WR. Impaired muscle oxygen use at onset of exercise in peripheral arterial disease. J Vasc Surg. 2004;40:488–93.CrossRefPubMed
30.
go back to reference Sako T, Hamaoka T, Higuchi H, Kurosawa Y, Katsumura T. Validity of NIR spectroscopy for quantitatively measuring muscle oxidative metabolic rate in exercise. J Appl Physiol (1985). 2001;90:338–44.CrossRef Sako T, Hamaoka T, Higuchi H, Kurosawa Y, Katsumura T. Validity of NIR spectroscopy for quantitatively measuring muscle oxidative metabolic rate in exercise. J Appl Physiol (1985). 2001;90:338–44.CrossRef
32.
go back to reference Kemp GJ, Roberts N, Bimson WE, et al. Mitochondrial function and oxygen supply in normal and in chronically ischemic muscle: a combined 31P magnetic resonance spectroscopy and near infrared spectroscopy study in vivo. J Vasc Surg. 2001;34:1103–1010.CrossRefPubMed Kemp GJ, Roberts N, Bimson WE, et al. Mitochondrial function and oxygen supply in normal and in chronically ischemic muscle: a combined 31P magnetic resonance spectroscopy and near infrared spectroscopy study in vivo. J Vasc Surg. 2001;34:1103–1010.CrossRefPubMed
33.
go back to reference Layec G, Hart CR, Trinity J, Le Fur Y, Jeong EK, Richardson R. Determinants of skeletal muscle work efficiency in patients with COPD. FASEB J. 2017;31:710–1. Layec G, Hart CR, Trinity J, Le Fur Y, Jeong EK, Richardson R. Determinants of skeletal muscle work efficiency in patients with COPD. FASEB J. 2017;31:710–1.
35.
go back to reference Belardinelli R, Barstow TJ, Porszasz J, Wasserman K. Changes in skeletal muscle oxygenation during incremental exercise measured with near infrared spectroscopy. Eur J Appl Physiol Occup Physiol. 1995;70:487–92.CrossRefPubMed Belardinelli R, Barstow TJ, Porszasz J, Wasserman K. Changes in skeletal muscle oxygenation during incremental exercise measured with near infrared spectroscopy. Eur J Appl Physiol Occup Physiol. 1995;70:487–92.CrossRefPubMed
36.
go back to reference Belardinelli R, Georgiou D, Barstow TJ. Near infrared spectroscopy and changes in skeletal muscle oxygenation during incremental exercise in chronic heart failure: a comparison with healthy subjects. G Ital Cardiol. 1995;25:715–24.PubMed Belardinelli R, Georgiou D, Barstow TJ. Near infrared spectroscopy and changes in skeletal muscle oxygenation during incremental exercise in chronic heart failure: a comparison with healthy subjects. G Ital Cardiol. 1995;25:715–24.PubMed
37.
go back to reference Tabira K, Horie J, Fujii H, et al. The relationship between skeletal muscle oxygenation and systemic oxygen uptake during exercise in subjects with COPD: a preliminary study. Respir Care. 2012;57:1602–10.CrossRefPubMed Tabira K, Horie J, Fujii H, et al. The relationship between skeletal muscle oxygenation and systemic oxygen uptake during exercise in subjects with COPD: a preliminary study. Respir Care. 2012;57:1602–10.CrossRefPubMed
39.
go back to reference Singh SJ, Morgan MD, Hardman AE, Rowe C, Bardsley PA. Comparison of oxygen uptake during a conventional treadmill test and the shuttle walking test in chronic airflow limitation. Eur Respir J. 1994;7:2016–20.PubMed Singh SJ, Morgan MD, Hardman AE, Rowe C, Bardsley PA. Comparison of oxygen uptake during a conventional treadmill test and the shuttle walking test in chronic airflow limitation. Eur Respir J. 1994;7:2016–20.PubMed
40.
go back to reference Arnardóttir RH, Emtner M, Hedenström H, Larsson K, Boman G. Peak exercise capacity estimated from incremental shuttle walking test in patients with COPD: a methodological study. Respir Res. 2006;7:127.CrossRefPubMedPubMedCentral Arnardóttir RH, Emtner M, Hedenström H, Larsson K, Boman G. Peak exercise capacity estimated from incremental shuttle walking test in patients with COPD: a methodological study. Respir Res. 2006;7:127.CrossRefPubMedPubMedCentral
42.
go back to reference McDermott MM, Guralnik JM, Ferrucci L, et al. Physical activity, walking exercise, and calf skeletal muscle characteristics in patients with peripheral arterial disease. J Vasc Surg. 2007;46:87–93.CrossRefPubMedPubMedCentral McDermott MM, Guralnik JM, Ferrucci L, et al. Physical activity, walking exercise, and calf skeletal muscle characteristics in patients with peripheral arterial disease. J Vasc Surg. 2007;46:87–93.CrossRefPubMedPubMedCentral
46.
go back to reference McCully KK, Iotti S, Kendrick K, et al. Simultaneous in vivo measurements of HbO2 saturation and PCr kinetics after exercise in normal humans. J Appl Physiol (1985). 1994;77:5–10.CrossRef McCully KK, Iotti S, Kendrick K, et al. Simultaneous in vivo measurements of HbO2 saturation and PCr kinetics after exercise in normal humans. J Appl Physiol (1985). 1994;77:5–10.CrossRef
47.
go back to reference Grassi B, Quaresima V, Marconi C, Ferrari M, Cerretelli P. Blood lactate accumulation and muscle deoxygenation during incremental exercise. J Appl Physiol (1985). 1999;87:348–55.CrossRef Grassi B, Quaresima V, Marconi C, Ferrari M, Cerretelli P. Blood lactate accumulation and muscle deoxygenation during incremental exercise. J Appl Physiol (1985). 1999;87:348–55.CrossRef
48.
go back to reference Costes F, Prieur F, Féasson L, Geyssant A, Barthélémy JC, Denis C. Influence of training on NIRS muscle oxygen saturation during submaximal exercise. Med Sci Sports Exerc. 2001;33:1484–9.CrossRefPubMed Costes F, Prieur F, Féasson L, Geyssant A, Barthélémy JC, Denis C. Influence of training on NIRS muscle oxygen saturation during submaximal exercise. Med Sci Sports Exerc. 2001;33:1484–9.CrossRefPubMed
49.
go back to reference Phypers B, Pierce JMT. Lactate physiology in health and disease. CEACCP. 2006;6:128–32. Phypers B, Pierce JMT. Lactate physiology in health and disease. CEACCP. 2006;6:128–32.
50.
go back to reference Bauer TA, Reusch JE, Levi M, Regensteiner JG. Skeletal muscle deoxygenation after the onset of moderate exercise suggests slowed microvascular blood flow kinetics in type 2 diabetes. Diabetes Care. 2007;30:2880–5.CrossRefPubMed Bauer TA, Reusch JE, Levi M, Regensteiner JG. Skeletal muscle deoxygenation after the onset of moderate exercise suggests slowed microvascular blood flow kinetics in type 2 diabetes. Diabetes Care. 2007;30:2880–5.CrossRefPubMed
51.
go back to reference Mohler ER III, Lech G, Supple GE, Wang H, Chance B. Impaired exercise-induced blood volume in type 2 diabetes with or without peripheral arterial disease measured by continuous-wave near-infrared spectroscopy. Diabetes Care. 2006;29:1856–9.CrossRefPubMed Mohler ER III, Lech G, Supple GE, Wang H, Chance B. Impaired exercise-induced blood volume in type 2 diabetes with or without peripheral arterial disease measured by continuous-wave near-infrared spectroscopy. Diabetes Care. 2006;29:1856–9.CrossRefPubMed
52.
go back to reference Sivitz WI, Yorek MA. Mitochondrial dysfunction in diabetes: from molecular mechanisms to functional significance and therapeutic opportunities. Antioxid Redox Signal. 2010;12:537–77.CrossRefPubMedPubMedCentral Sivitz WI, Yorek MA. Mitochondrial dysfunction in diabetes: from molecular mechanisms to functional significance and therapeutic opportunities. Antioxid Redox Signal. 2010;12:537–77.CrossRefPubMedPubMedCentral
55.
go back to reference Meznar M, Pareznik R, Voga F. Effect of anemia on tissue oxygenation saturation and the tissue deoxygenation rate during ischemia. Crit Care. 2009;13:238.CrossRef Meznar M, Pareznik R, Voga F. Effect of anemia on tissue oxygenation saturation and the tissue deoxygenation rate during ischemia. Crit Care. 2009;13:238.CrossRef
56.
go back to reference Cooper CE, Penfold SM, Elwell CE, Angus C. Comparison of local adipose tissue content and SRS-derived NIRS muscle oxygenation measurements in 90 individuals. In: Takahashi E, Bruley DF, editors. Oxygen transport to tissue XXXI. Advances in experimental medicine and biology. Berlin: Springer; 2010. pp. 177–81.CrossRef Cooper CE, Penfold SM, Elwell CE, Angus C. Comparison of local adipose tissue content and SRS-derived NIRS muscle oxygenation measurements in 90 individuals. In: Takahashi E, Bruley DF, editors. Oxygen transport to tissue XXXI. Advances in experimental medicine and biology. Berlin: Springer; 2010. pp. 177–81.CrossRef
Metadata
Title
Characterising skeletal muscle haemoglobin saturation during exercise using near-infrared spectroscopy in chronic kidney disease
Authors
Thomas J. Wilkinson
Alice E. M. White
Daniel G. D. Nixon
Douglas W. Gould
Emma L. Watson
Alice C. Smith
Publication date
01-01-2019
Publisher
Springer Singapore
Published in
Clinical and Experimental Nephrology / Issue 1/2019
Print ISSN: 1342-1751
Electronic ISSN: 1437-7799
DOI
https://doi.org/10.1007/s10157-018-1612-0

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