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BMC Sports Science, Medicine and Rehabilitation

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Open Access 01-12-2024 | Research

A systematic review of the relationship between muscle oxygen dynamics and energy rich phosphates. Can NIRS help?

Authors: Kevin Maliszewski, Andri Feldmann, Kevin K. McCully, Ross Julian

Published in: BMC Sports Science, Medicine and Rehabilitation | Issue 1/2024

Abstract

Background

Phosphocreatine dynamics provide the gold standard evaluation of in-vivo mitochondrial function and is tightly coupled with oxygen availability. Low mitochondrial oxidative capacity has been associated with health issues and low exercise performance.

Methods

To evaluate the relationship between near-infrared spectroscopy-based muscle oxygen dynamics and magnetic resonance spectroscopy-based energy-rich phosphates, a systematic review of the literature related to muscle oxygen dynamics and energy-rich phosphates was conducted. PRISMA guidelines were followed to perform a comprehensive and systematic search of four databases on 02-11-2021 (PubMed, MEDLINE, Scopus and Web of Science). Beforehand pre-registration with the Open Science Framework was performed. Studies had to include healthy humans aged 18–55, measures related to NIRS-based muscle oxygen measures in combination with energy-rich phosphates. Exclusion criteria were clinical populations, laboratory animals, acutely injured subjects, data that only assessed oxygen dynamics or energy-rich phosphates, or grey literature. The Effective Public Health Practice Project Quality Assessment Tool was used to assess methodological quality, and data extraction was presented in a table.

Results

Out of 1483 records, 28 were eligible. All included studies were rated moderate. The studies suggest muscle oxygen dynamics could indicate energy-rich phosphates under appropriate protocol settings.

Conclusion

Arterial occlusion and exercise intensity might be important factors to control if NIRS application should be used to examine energetics. However, more research needs to be conducted without arterial occlusion and with high-intensity exercises to support the applicability of NIRS and provide an agreement level in the concurrent course of muscle oxygen kinetics and muscle energetics.

Trial registration

https://osf.io/py32n/.

Key points

1. NIRS derived measures of muscle oxygenation agree with gold-standard measures of high energy phosphates when assessed in an appropriate protocol setting.

2. At rest when applying the AO protocol, in the absence of muscle activity, an initial disjunction between the NIRS signal and high energy phosphates can been seen, suggesting a cascading relationship.

3. During exercise and recovery a disruption of oxygen delivery is required to provide the appropriate setting for evaluation through either an AO protocol or high intensity contractions.

Popov V, Medvedev NI, Davies HA, Stewart MG. Mitochondria form a filamentous reticular network in hippocampal dendrites but are present as discrete bodies in axons: a three-dimensional ultrastructural study. J Comp Neurol. 2005;492(1):50–65.PubMedCrossRef

Willingham TB, Ajayi PT, Glancy B. Subcellular specialization of mitochondrial form and function in skeletal muscle cells. Front cell Dev Biol. 2021;9:757305.PubMedPubMedCentralCrossRef

Connett RJ, Honig CR, Gayeski TE, Brooks GA. Defining hypoxia: a systems view of VO2, glycolysis, energetics, and intracellular PO2. J Appl Physiol. 1990;68(3):833–42.PubMedCrossRef

Shulman RG, Rothman DL. The “glycogen shunt” in exercising muscle: a role for glycogen in muscle energetics and fatigue. Proc Natl Acad Sci U S A. 2001;98(2):457–61.PubMedPubMedCentralCrossRef

Hamaoka T, McCully KK, Quaresima V, Yamamoto K, Chance B. Near-infrared spectroscopy/imaging for monitoring muscle oxygenation and oxidative metabolism in healthy and diseased humans. J Biomed Opt. 2007;12(6):062105.PubMedCrossRef

Ryan TE, Southern WM, Reynolds MA, McCully KK. A cross-validation of near-infrared spectroscopy measurements of skeletal muscle oxidative capacity with phosphorus magnetic resonance spectroscopy. J Appl Physiol. 2013;115(12):1757–66.PubMedPubMedCentralCrossRef

Ryan TE, Brophy P, Te LC, Hickner RC, Neufer PD. Assessment of in vivo skeletal muscle mitochondrial respiratory capacity in humans by near-infrared spectroscopy: a comparison with in situ measurements. J Physiol. 2014;592(15):3231–41.PubMedPubMedCentralCrossRef

Grassi B, Quaresima V, Marconi C, Ferrari M, Cerretelli P. Blood lactate accumulation and muscle deoxygenation during incremental exercise. J Appl Physiol. 1999;87(1):348–55.PubMedCrossRef

Kemp GJ, Ahmad RE, Nicolay K, Prompers JJ. Quantification of skeletal muscle mitochondrial function by 31 P magnetic resonance spectroscopy techniques: a quantitative review. Acta Physiol. 2015;213(1):107–44.CrossRef

10.

Haseler LJ, Hogan MC, Richardson RS. Skeletal muscle phosphocreatine recovery in exercise-trained humans is dependent on O2 availability. J Appl Physiol. 1999;86(6):2013–8.PubMedCrossRef

11.

Mader A, Heck H. A theory of the metabolic origin of “anaerobic thresold.” Int J Sports Med. 1986;7(1):45–65.PubMedCrossRef

12.

Brand MD. Regulation analysis of energy metabolism. J Exp Biol. 1997;200(Pt 2):193–202.PubMedCrossRef

13.

Mahler M. First-order kinetics of muscle oxygen consumption, and an equivalent proportionality between QO2 and phosphorylcreatine level. Implications for the control of respiration. J Gen Physiol. 1985;86(1):135–65.PubMedCrossRef

14.

Meyer RA. A linear model of muscle respiration explains monoexponential phosphocreatine changes. Am J Phys. 1988;254(4):548–53.

15.

Holloszy JO, Coyle EF. Adaptations of skeletal muscle to endurance exercise and their metabolic consequences. J Appl Physiol. 1984;56(4):831–8.PubMedCrossRef

16.

Gollnick PD, Armstrong RB, Saltin B, Saubert CW, Sembrowich WL, Shepherd RE. Effect of training on enzyme activity and fiber composition of human skeletal muscle. J Appl Physiol. 1973;34(1):107–11.PubMedCrossRef

17.

Fryer S, Stoner L, Stone K, Giles D, Sveen J, Garrido I, et al. Forearm muscle oxidative capacity index predicts sport rock-climbing performance. Eur J Appl Physiol. 2016;116(8):1479–84.PubMedCrossRef

18.

Nakada M, Demura S, Yamaji S, Minami M, Kitabayashi T, Nagasawa Y. Relationships between force curves and muscle oxygenation kinetics during repeated handgrip. J Physiol Anthropol Appl Hum Sci. 2004;23(6):191–6.CrossRef

19.

Philippe M, Wegst D, Müller T, Raschner C, Burtscher M. Climbing-specific finger flexor performance and forearm muscle oxygenation in elite male and female sport climbers. Eur J Appl Physiol. 2012;112(8):2839–47.PubMedCrossRef

20.

van der Zwaard S, Jaspers RT, Blokland IJ, Achterberg C, Visser JM, den Uil AR, et al. Oxygenation Threshold Derived from Near-Infrared Spectroscopy: Reliability and Its Relationship with the First Ventilatory Threshold. Fisher G, editor. PLoS One. 2016;11(9).

21.

Perrey S, Ferrari M. Muscle oximetry in sports science: a systematic review. Sport Med. 2018;48(3):597–616.CrossRef

22.

McCully KK, Iotti S, Kendrick K, Wang Z, Posner JD, Leigh JJ, et al. Simultaneous in vivo measurements of HbO2 saturation and PCr kinetics after exercise in normal humans. J Appl Physiol. 1994;77(1):5–10.PubMedCrossRef

23.

Campbell MD, Marcinek DJ. Evaluation of in vivo mitochondrial bioenergetics in skeletal muscle using NMR and optical methods. Biochim Biophys Acta - Mol Basis Dis. 2016;1862(4):716–24.CrossRef

24.

Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gøtzsche PC, Ioannidis JPA, et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. PLoS Med. 2009;6.

25.

Hamaoka T, McCully KK. Review of early development of near-infrared spectroscopy and recent advancement of studies on muscle oxygenation and oxidative metabolism. J Physiol Sci. 2019;69(6):799–811.PubMedPubMedCentralCrossRef

26.

Hamaoka T, Iwane H, Shimomitsu T, Katsumura T, Murase N, Nishio S, et al. Noninvasive measures of oxidative metabolism on working human muscles by near-infrared spectroscopy. J Appl Physiol. 1996;81(3):1410–7.PubMedCrossRef

27.

Yoshida T, Watari H, Tagawa K. Effects of active and passive recoveries on splitting of the inorganic phosphate peak determined by 31P-nuclear magnetic resonance spectroscopy. NMR Biomed. 1996;9(1):13–9.PubMedCrossRef

28.

Binzoni T, Hiltbrand E. Influence of repeated ischaemia/reperfusion cycles (ischaemic preconditioning) on human calf energy metabolism by simultaneous near infrared spectroscopy,31P-NMR and 23Na-NMR measurements. Adv Exp Med Biol. 1997;428:533–8.PubMedCrossRef

29.

Binzoni T, Quaresima V, Barattelli G, Hiltbrand E, Gürke L, Terrier F, et al. Energy metabolism and interstitial fluid displacement in human gastrocnemius during short ischemic cycles. J Appl Physiol. 1998;85(4):1244–51.PubMedCrossRef

30.

Boushel R, Pott F, Madsen P, Rådegran G, Nowak M, Quistorff B, et al. Muscle metabolism from near infrared spectroscopy during rhythmic handgrip in humans. Eur J Appl Physiol Occup Physiol. 1998;79(1):41–8.PubMedCrossRef

31.

Kutsuzawa T, Shioya S, Kurita D, Haida M, Yamabayashi H. Effects of age on muscle energy metabolism and oxygenation in the forearm muscles. Med Sci Sports Exerc. 2001;33(6):901–6.PubMedCrossRef

32.

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. 2001;90(1):338–44.PubMedCrossRef

33.

Hamaoka T, Katsumura T, Murase N, Sako T, Higuchi H, Murakami M, et al. Muscle oxygen consumption at onset of exercise by near infrared spectroscopy in humans. In: Advances in experimental medicine and biology. Kluwer Academic/Plenum Publishers; 2003. p. 475–83.

34.

Kime R, Hamaoka T, Sako T, Murakami M, Homma T, Katsumura T, et al. Delayed reoxygenation after maximal isometric handgrip exercise in high oxidative capacity muscle. Eur J Appl Physiol. 2003;89(1):34–41.PubMedCrossRef

35.

Kime R, Katsumura T, Hamaoka T, Osada T, Sako T, Murakami M, et al. In: Dunn JF, Swartz HM, editors., et al., Muscle Reoxygenation rate after isometric exercise at various intensities in relation to muscle oxidative capacity BT - oxygen transport to tissue XXIV. Boston, MA: Springer US; 2003. p. 497–507.

36.

Nagasawa T, Hamaoka T, Sako T, Murakami M, Kime R, Homma T, et al. A practical indicator of muscle oxidative capacity determined by recovery of muscle O2 consumption using NIR spectroscopy. Eur J Sport Sci. 2003;3(2):1–10.CrossRef

37.

Forbes SC, Kowalchuk JM, Thompson RT, Marsh GD. Effects of hyperventilation on phosphocreatine kinetics and muscle deoxygenation during moderate-intensity plantar flexion exercise. J Appl Physiol. 2007;102(4):1565–73.PubMedCrossRef

38.

Kimura N, Hamaoka T, Kurosawa Y, Katsumura T. Contribution of intramuscular oxidative metabolism to Total ATP production during forearm isometric exercise at varying intensities. Tohoku J Exp Med. 2006;208(4):307–20.PubMedCrossRef

39.

Jones AM, Fulford J, Wilkerson DP. Influence of prior exercise on muscle [phosphorylcreatine] and deoxygenation kinetics during high-intensity exercise in men. Exp Physiol. 2008;93(4):468–78.PubMedCrossRef

40.

Forbes SC, Raymer GH, Kowalchuk JM, Thompson RT, Marsh GD. Effects of recovery time on phosphocreatine kinetics during repeated bouts of heavy-intensity exercise. Eur J Appl Physiol. 2008;103(6):665–75.PubMedCrossRef

41.

Zange J, Beisteiner M, Müller K, Shushakov V, Maassen N. Energy metabolism in intensively exercising calf muscle under a simulated orthostasis. Pflugers Arch Eur J Physiol. 2008;455(6):1153–63.CrossRef

42.

Layec G, Bringard A, Le Fur Y, Vilmen C, Micallef JP, Perrey S, et al. Effects of a prior high-intensity knee-extension exercise on muscle recruitment and energy cost: a combined local and global investigation in humans. Exp Physiol. 2009;94(6):704–19.PubMedCrossRef

43.

Willcocks RJ, Williams CA, Barker AR, Fulford J, Armstrong N. Age- and sex-related differences in muscle phosphocreatine and oxygenation kinetics during high-intensity exercise in adolescents and adults. NMR Biomed. 2010;23(6):569–77.PubMedCrossRef

44.

Layec G, Bringard A, Yashiro K, Le Fur Y, Vilmen C, Micallef JP, et al. The slow components of phosphocreatine and pulmonary oxygen uptake can be dissociated during heavy exercise according to training status. Exp Physiol. 2012;97(8):955–69.PubMedCrossRef

45.

Layec G, Haseler LJ, Trinity JD, Hart CR, Liu X, Le Fur Y, et al. Mitochondrial function and increased convective O-2 transport: implications for the assessment of mitochondrial respiration in vivo. J Appl Physiol. 2013;115(6):803–11.PubMedPubMedCentralCrossRef

46.

Fulford J, Liepa A, Barker AR, Meakin J. The reliability of 31P-MRS and NIRS measurements of spinal muscle function. Int J Sports Med. 2014;35(13):1078–83.PubMedCrossRef

47.

Hart CR, Layec G, Trinity JD, Liu X, Kim S-E, Groot HJ, et al. Evidence of preserved oxidative capacity and oxygen delivery in the plantar flexor muscles with age. J Gerontol Ser A Biol Sci Med Sci. 2015;70(9):1067–76.CrossRef

48.

Layec G, Trinity JD, Hart CR, Kim SE, Groot HJ, Le Fur Y, et al. In vivo evidence of an age-related increase in ATP cost of contraction in the plantar flexor muscles. Clin Sci. 2014;126(8):581–92.CrossRef

49.

Bendahan D, Chatel B, Jue T. Comparative NMR and NIRS analysis of oxygen-dependent metabolism in exercising finger flexor muscles. Am J Physiol - Regul Integr Comp Physiol. 2017;313(6):R740–53.PubMedPubMedCentralCrossRef

50.

Yanagisawa O, Sanomura M. Effects of low-load resistance exercise with blood flow restriction on high-energy phosphate metabolism and oxygenation level in skeletal muscle. Interv Med Appl Sci. 2017;9(2):67–75.PubMedPubMedCentral

51.

Heskamp L, Lebbink F, van Uden MJ, Maas MC, Claassen JAHR, Froeling M, et al. Post-exercise intramuscular O2 supply is tightly coupled with a higher proximal-to-distal ATP synthesis rate in human tibialis anterior. J Physiol. 2020;599(5):1533–50.CrossRef

52.

Zange J, Haller T, Müller K, Liphardt AM, Mester J. Energy metabolism in human calf muscle performing isometric plantar flexion superimposed by 20-Hz vibration. Eur J Appl Physiol. 2009;105(2):265–70.PubMedCrossRef

53.

Mann CJ. Observational research methods. Research design II: cohort, cross sectional, and case-control studies. Emerg Med J. 2003;20(1):54–60.PubMedPubMedCentralCrossRef

54.

Chuang M-L, Ting H, Otsuka T, Sun X-G, Chiu FY-L, Hansen JE, et al. Muscle deoxygenation as related to work rate. Med Sci Sports Exerc. 2002;34(10):1614–23.PubMedCrossRef

55.

Connett RJ, Gayeski TE, Honig CR. Energy sources in fully aerobic rest-work transitions: a new role for glycolysis. Am J Physiol Circ Physiol. 1985;248(6):922–9.CrossRef

56.

Robergs RA, Ghiasvand F, Parker D. Biochemistry of exercise-induced metabolic acidosis. Am J Physiol Integr Comp Physiol. 2004;287(3):502–16.CrossRef

57.

Barbiroli B, Iotti S, Lodi R. Aspects of human bioenergetics as studied in vivo by magnetic resonance spectroscopy. Biochimie. 1998;80(10):847–53.PubMedCrossRef

58.

McMahon S, Jenkins D. Factors affecting the rate of phosphocreatine Resynthesis following intense exercise. Sport Med. 2002;32(12):761–84.CrossRef

59.

Chilibeck PD, Paterson DH, Petrella RJ, Cunningham DA. The influence of age and cardiorespiratory fitness on kinetics of oxygen uptake. Can J Appl Physiol. 1996;21(3):185–96.PubMedCrossRef

60.

Ren J, Lakoski S, Haller RG, Sherry AD, Malloy CR. Dynamic monitoring of carnitine and acetylcarnitine in the trimethylamine signal after exercise in human skeletal muscle by 7T 1H-MRS. Magn Reson Med. 2013;69(1):7–17.PubMedCrossRef

61.

Damon BM, Buck AKW, Ding Z. Diffusion-tensor MRI based skeletal muscle Fiber tracking. Imaging Med. 2011;3(6):675–87.PubMedPubMedCentralCrossRef

62.

DeBrosse C, Nanga RPR, Wilson N, D’Aquilla K, Elliott M, Hariharan H, et al. Muscle oxidative phosphorylation quantitation using creatine chemical exchange saturation transfer (CrCEST) MRI in mitochondrial disorders. JCI insight. 2016;1(18):e88207.PubMedPubMedCentralCrossRef

Title: A systematic review of the relationship between muscle oxygen dynamics and energy rich phosphates. Can NIRS help?
Authors: Kevin Maliszewski
Andri Feldmann
Kevin K. McCully
Ross Julian
Publication date: 01-12-2024
Publisher: BioMed Central
Published in: BMC Sports Science, Medicine and Rehabilitation / Issue 1/2024
Electronic ISSN: 2052-1847
DOI: https://doi.org/10.1186/s13102-024-00809-5

Keynote webinar | Spotlight on medication adherence

Springer Medicine

A systematic review of the relationship between muscle oxygen dynamics and energy rich phosphates. Can NIRS help?

Abstract

Background

Methods

Results

Conclusion

Trial registration

Key points

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Background

Methods

Results

Conclusion

Trial registration

Key points

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