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Muscle cooling modulates tissue oxidative and biochemical responses but not energy metabolism during exercise

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Abstract

Purpose

This study investigated whether muscle cooling and its associated effects on skeletal muscle oxidative responses, blood gases, and hormonal concentrations influenced energy metabolism during cycling.

Methods

Twelve healthy participants (Males: seven; Females: five) performed two steady-state exercise sessions at 70% of ventilatory threshold on a cycle ergometer. Participants completed one session with pre-exercise leg cooling until muscle temperature (Tm) decreased by 6 °C (LCO), and a separate session without cooling (CON). They exercised until Tm returned to baseline and for an additional 30 min. Cardiovascular, respiratory, metabolic, hemodynamic variables, and skeletal muscle tissue oxidative responses were assessed continuously. Venous blood samples were collected to assess blood gases, and hormones.

Results

Heart rate, stroke volume, and cardiac output all increased across time but were not different between conditions. V̇O2 was greater in LCO when muscle temperature was restored until the end of exercise (p < 0.05). Cycling in the LCO condition induced lower oxygen availability, tissue oxygenation, blood pH, sO2%, and pO2 (p < 0.05). Insulin concentrations were also higher in LCO vs. CON (p < 0.05). Importantly, stoichiometric equations from respiratory gases indicated no differences in fat and CHO oxidation between conditions.

Conclusion

The present study demonstrated that despite muscle cooling and the associated oxidative and biochemical changes, energy metabolism remained unaltered during cycling. Whether lower local and systemic oxygen availability is counteracted via a cold-induced activation of lipid metabolism pathways needs to be further investigated.

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Abbreviations

%TSI:

Percentage tissue saturation index

CHO:

Carbohydrates

CPT-1:

Carnitine palmitoyl transferase-I

diffHb:

Difference oxy/deoxygenated hemoglobin

HHb:

Deoxygenated hemoglobin

NIRS:

Near-infrared spectrometry

O2Hb:

Oxygenated hemoglobin

PCO2 :

Partial pressure of carbon dioxide

PO2 :

Partial pressure of oxygen

RER:

Respiratory exchange ratio

tHb:

Total hemoglobin

T c :

Core temperature

T m :

Muscle temperature

T̅ sk :

Mean weighted skin temperature

V̇E:

Minute ventilation

VL:

Vastus lateralis

VT:

Ventilatory threshold

V t :

Tidal volume

V̇O2peak :

Peak oxygen consumption

V̇O2 :

Rate of oxygen consumption

V̇CO2 :

Rate of carbon dioxide release

W :

Watts

References

  • Alston T (2004) Blood gases and pH during hypothermia: the ‘Stats’. Int Anesth Clin 42(4):73–80

    Google Scholar 

  • Bacher A (2005) Effect of body temperature on blood gases. Int Care Med 31:24–27

    Google Scholar 

  • Beelen A, Sargeant AJ (1991) Effect of lowered muscle temperature on the physiology response to exercise in men. Eur J Appl Physiol 63:387–392

    CAS  Google Scholar 

  • Bennett AF (1984) Thermal dependence of muscle function. Am J Physiol Regul Integr Comp Physiol 247(2):R217–R229

    CAS  Google Scholar 

  • Bennett AF (1985) Temperature and muscle. J Exp Biol 115:333–344

    CAS  PubMed  Google Scholar 

  • Brosek JF, Grande JT, Andersen JT, Keys A (1963) Densiometric analysis of body composition: review of some quantitative assumptions. Ann NY Acad Sci 110:113–140

    Google Scholar 

  • Bylund-Fellenius AC, Walker PM, Elander A, Holm S, Holm J, Schersten T (1981) Energy metabolism in relation to oxygen partial pressure in human skeletal muscle during exercise. Biochem J 200:247–255

    CAS  PubMed  PubMed Central  Google Scholar 

  • Charloux A, Lonsdorfer-Wolf E, Richard R, Lampert E, Oswald-Mammosser M et al (2000) A new impedance cardiograph device for the non-invasive evaluation of cardiac output at rest and during exercise: comparison with the direct Fick method. Eur J Appl Physiol 82(4):313–320

    CAS  PubMed  Google Scholar 

  • Chiesa ST, Trangmar SJ, Gonzalez-Alonso J (2016) Temperature and blood flow distribution in the human leg during passive heat stress. J Appl Physiol 120(9):1047–1058

    PubMed  PubMed Central  Google Scholar 

  • Coggins M, Lindner J, Rattigan S, Jahn L, Fasy E, Kaul S et al (2001) Physiologic hyperinsulinemia enhances human skeletal muscle perfusion by capillary recruitment. Diabetes 50(12):2682–2690

    CAS  PubMed  Google Scholar 

  • Deban SM, Lappin AK (2011) The effects on the dynamics and motor control of ballistic prey capture in toads: maintaining high performance at low temperature. J Exp Biol 214:1333–1346

    PubMed  Google Scholar 

  • DuBois DF (1916) A formula to estimate the approximate surface area if height and body mass be known. Arch Intern Med 17:836–871

    Google Scholar 

  • Febbraio MA, Snow RJ, Stathis CG, Hargreaves M, Carey M (1996) Blunting the rise in body temperature reduces muscle glycogenolysis during exercise in humans. Exp Physiol 81:685–693

    CAS  PubMed  Google Scholar 

  • Fink WJ, Costill DL, Van Handel PJ (1975) Leg muscle metabolism during exercise in the heat and cold. Eur J Appl Physiol 34(3):183–190

    CAS  Google Scholar 

  • Frank SM, Higgins MS, Fleisher LA, Sitzmann JV, Raff H, Breslow MJ (1997) Adrenergic, respiratory, and cardiovascular effects of core cooling in humans. Am J Physiol Regul Integr Comp Physiol 272(2):R557–R562

    CAS  Google Scholar 

  • Freedman RR, Sabharwal SC, Moten M, Migaly P (1992) Local temperature modulates α1- and α2-adrenergic vasoconstriction in men. Heart Circ Physiol 32:H1197–1200

    Google Scholar 

  • Gagnon DD, Rintamäki H, Gagnon SS, Cheung SS, Herzig K-H, Porvari K, Kyröläinen H (2013) Cold exposure enhances fat utilization but not non-esterified fatty acids, glycerol or catecholamines availability during submaximal walking and running. Front Physiol. https://doi.org/10.3389/fphys.2013.00099

    Article  PubMed  PubMed Central  Google Scholar 

  • Gagnon DD, Gagnon SS, Rintamäki H, Törmäkangas T, Puukka K, Herzig KH, Kyröläinen H (2014) The effects of cold exposure on leukocytes, hormones and cytokines during acute exercise in humans. PLoS ONE 9(10):110774

    Google Scholar 

  • Gagnon DD, Peltonen JE, Rintamäki H, Gagnon SS, Herzig KH, Kyröläinen H (2017) The effects of skin and core tissue cooling on oxygenation of the vastus lateralis muscle during walking and running. J Sports Sci 35(20):1995–2004

    PubMed  Google Scholar 

  • Gagnon DD, Perrier L, Dorman S, Oddson B, Larivière C, Serresse O (2020) Ambient temperature inifluence metabolic substrate oxidation curves during running and cycling in healthy men. Eur J Sport Sci 20(1):90–99. https://doi.org/10.1080/17461391.2019.1612949

    Article  PubMed  Google Scholar 

  • Gasparetti AL, de Souza CT, Pereira-da-Silva M, Oliveira RL, Saad MJ, Carneiro EM, Velloso LA (2003) Cold exposure induces tissue-specific modulation of the insulin-signalling pathway in Rattus norvegicus. J Physiol 552(1):149–162

    CAS  PubMed  PubMed Central  Google Scholar 

  • Goodman AH, Einstein R, Granger HJ (1978) Effect of changing metabolic rate on local blood flow control in the canine hind limb. Circ Res 43:769–776

    CAS  PubMed  Google Scholar 

  • Gordon N, Abbiss C, Maiorana A, Marston K, Peiffer J (2018) Interrater reliability and agreement of the Physioflow bioimpedance cardiography device during rest, moderate and high-intensity exercise. Kinesiology 50:140–149

    Google Scholar 

  • Granger HJ, Goodman AH, Granger DN (1976) Role of resistance and exchange vessels in local microvascular control of skeletal muscle oxygenation in the dog. Circ Res 38:379–385

    CAS  PubMed  Google Scholar 

  • Haycock GB, Schwartz GJ, Wisotsky DH (1978) Geometric method for measuring body surface area: a height-weight formula validated in infants, children, and adults. J Pediat 93(1):62–66

    CAS  PubMed  Google Scholar 

  • Heinonen I, Btothers RM, Kemppainen J, Knuuti J, Kalliokoski KK, Crandall GG (2011) Local heating, but not indirect whole body heating, increases human skeletal muscle blood flow. J Appl Physiol 111(3):818–824

    PubMed  PubMed Central  Google Scholar 

  • Heinonen I, Koga S, Kalliokoski KK, Musch TI, Poole DC (2015) Heterogeneity of muscle blood flow and metabolism: influence of exercise, aging and disease state. Exerc Sport Sci Rev 43(3):117–124

    PubMed  PubMed Central  Google Scholar 

  • Heinonen I, Saltin B, Hellsten Y, Kalliokoski KK (2017) The effect of nitric oxide synthase inhibition with and without inhibition of prostaglandins on blood flow in different human skeletal muscles. Eur J Appl Physiol 117(6):1175–1180

    CAS  PubMed  Google Scholar 

  • Hiramatsu K, Yamada T, Katakura M (1984) Acute effects of cold on blood pressure, renin-angiotensin-aldosterone system, catecholamines and adrenal steroids in man. Clin Exp Pharmacol Physiol 11(2):171–179

    CAS  PubMed  Google Scholar 

  • Honig CR, Odoroff CL, Frierson JL (1980) Capillary recruitment in exercise: rate, extent, uniformity, and relation to blood flow. Am J Physiol 238:H31–H42

    CAS  PubMed  Google Scholar 

  • Honig CR, Odoroff CL, Frierson JL (1982) Active and passive capillary control in red muscle at rest and in exercise. Am J Physiol 243:H196–H206

    CAS  PubMed  Google Scholar 

  • Hoy A, McLennan PL, Peoples GE (2009) The effect of vasoconstrictors on oxygen consumption in resting and contracting skeletal muscle of the autologous pump-perfused rat hindlimb. J Physiol Pharma 60(3):155

    CAS  Google Scholar 

  • Hudlicka O (1985) Regulation of muscle blood flow. Clin Physiol 5:201–229

    CAS  PubMed  Google Scholar 

  • Idström JP, Harihara Subramanian V, Chance B, Schersten T, Bylund-Fellenius AC (1985) Oxygen dependence of energy metabolism in contracting and recovering rat skeletal muscle. Heart Circ Physiol 17:H40–H48

  • Ihsan M, Watson G, Lipski M, Abbiss CR (2013) Influence of postexercise cooling on muscle oxygenation and blood volume changes. Med Sci Sports Exerc 45(5):876–882

    CAS  PubMed  Google Scholar 

  • Jeacocke NA, Burke LM (2010) Methods to standardize dietary intake before performance testing. Int J Sport Nutr Exerc Metab 20:87–103

    CAS  PubMed  Google Scholar 

  • Jeukendrup AE, Wallis GA (2005) Measurement of substrate oxidation during exercise by means of gas exchange measurements. Int J Sports Med 28:528–537

    Google Scholar 

  • Johnson JM, Kellog DL (2010) Local thermal control of the human cutaneous circulation. J Appl Physiol 109:1229–1238

    PubMed  PubMed Central  Google Scholar 

  • Johnson DG, Hayward JS, Jacobs TP, Collis ML, Eckerson JD, Williams RH (1977) Plasma norepinephrine responses of man in cold water. J Appl Physiol 43(2):216–220

    CAS  PubMed  Google Scholar 

  • Johnson JM, Minson CT, Kellog DL (2014) Cutaneous vasodilation and vasoconstrictor mechanism in temperature regulation. Comp Physiol 4(1):33–89

    Google Scholar 

  • Kamariah Binti Md I, Kawasaki N, Ueyama K, Sumii T, Kodu S (2011) Effects of cold exposure and shear stress on endothelial nitric oxide synthase activation. Biochem Biophys Res Comm 412:318–322

    Google Scholar 

  • Krogh A (1919) The supply of oxygen to the tissues and the regulation of the capillary circulation. J Physiol 52(6):457–474

    CAS  PubMed  PubMed Central  Google Scholar 

  • Loenneke JP, Kim D, Fahs CA, Thiebaud RS, Abe T, Larson RD, Bemben DA, Bemben MG (2017) The influence of exercise load with and without different levels of blood flow restriction on acute changes in muscle thickness and lactate. Clin Physiol Funct Imaging 37(6):734–740

    CAS  PubMed  Google Scholar 

  • Mairbäurl H, Humpeler E (1980) Diminution of the temperature effects on the oxygen affinity of hemoglobin after prolonged hypothermia. Pflug Arch 383(3):209–213

    Google Scholar 

  • Mancini DM, Bolinger L, Li H, Kendrick K, Chance B, Wilson JR (1994) Validation of near-infrared spectroscopy in humans. J Appl Physiol 77:2740–2747

    CAS  PubMed  Google Scholar 

  • McCully KK, Smith S, Rajaei S, Leigh JS Jr, Natelson BH (2004) Muscle metabolism with blood flow restriction in chronic fatigue syndrome. J Appl Physiol 96:871–878

    PubMed  Google Scholar 

  • Murias JM, Spencer MD, Keir DA, Paterson DH (2013) Systemic and vastus lateralis muscle blood flow and O2 extraction during ramp incremental cycle exercise. AJP Regul Integr Comp Physiol 304(9):R720–R725

    CAS  Google Scholar 

  • O’Malley BP, Cook N, Richardson A, Barnett DB, Rosenthal FD (1984) Circulating catecholamines, thyrotrophin, thryroind hormone and prolactin responses of normal subjects to acute cold exposure. Clin Endocrinol 21:285–291

    Google Scholar 

  • Oksa J, Kaikkonen H, Sorvisto P, Vaappo M, Martikkala V, Rintamaki H (2004) Changes in maximal cardiorespiratory capacity and submaximal strain while exercising in the cold. J Therm Biol 29:815–818

    Google Scholar 

  • Orava J, Muutila P, Lidell ME, Oikonen V, Noponen T, Viljanen T et al (2011) Different metabolic responses of human brown adipose tissue to activation of cold and insulin. Cell Metab 14:272–279

    CAS  PubMed  Google Scholar 

  • Palmes ED, Park CR (1948) An improved mounting for thermocouples for the measurement of the surface temperature of the body. J Lab Clin Med 33(8):1044–1046

    CAS  PubMed  Google Scholar 

  • Pearson J, Low DA, Stöhr E, Kalsi K, Ali L, Barker H, Gonzalez-Alonso J (2011) Hemodynamic responses to heat stress in the resting and exercising human leg: insight on the effect of temperature on skeletal muscle blood flow. Am J Physiol Regul Integr Comp Physiol 300(3):R663–R673

    CAS  PubMed  Google Scholar 

  • Richard R, Lonsdorfer-Wolf E, Charloux A, Doutreleau S, Buchheit M, Oswald-Mammosser M et al (2001) Non-invasive cardiac output evaluation during a maximal progressive exercise test, using a new impedance cardiograph device. Eur J Appl Physiol 85(3–4):202–207

    CAS  PubMed  Google Scholar 

  • Roberts CK, Barnard RJ, Jasman A, Balon TW (1999) Acute exercise increases nitric oxide synthase activity in skeletal muscle. Endocrinol Metab 40:E-390–E-394

    Google Scholar 

  • Rosenmeier JB, Hansen J, Gonzalez-Alonso J (2004) Circulating ATP-induced vasodilation overrides sympathetic vasoconstrictor activity in human skeletal muscle. J Physiol 558(1):351–365

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sasaki Y, Takahashi H, Aso H, Ohneda A, Weekes TE (1982) Effects of cold exposure on insulin and glucagon secretion in sheep. Endocrinology 111(6):2070–2076

    CAS  PubMed  Google Scholar 

  • Segal S (2005) Regulation of blood flow in the microcirculation. Microcirculation 12:33–45

    PubMed  Google Scholar 

  • Sheeren TWL, Schober P, Schwarte LA (2012) Monitoring tissue oxygenation by near infrared spectroscopy (NIRS): background and current applications. J Clin Monit Comput 26:279–287

    Google Scholar 

  • Sidell BD (1998) Intracellular oxygen diffusion: the roles of myoglobin and lipid at cold body temperature. J Exp Biol 201:1118–1127

    Google Scholar 

  • Siggaard-Andersen O, Wimberley PD, Göthgen I, Siggaard-Andersen M (1984) A mathematical model of the hemoglobin-oxygen dissociation curve of human blood and of the oxygen partial pressure as a function of temperature. Clin Chem 30(10):1646–1651

    CAS  PubMed  Google Scholar 

  • Starkie RL, Hargreaves M, Lambert DL, Proietto J, Febbraio M (1999) Effect of temperature on muscle metabolism during submaximal exercise in humans. Exp Physiol 84(4):775–784

    CAS  PubMed  Google Scholar 

  • Thomas GD, Segal SS (2004) Neural control of muscle blood flow during exercise. J Appl Physiol 97:731–738

    CAS  PubMed  Google Scholar 

  • Thompson-Torgerson CS, Holowatz LA, Flavahan NA, Kenney WL (2007) Cold-induced cutaneous vasoconstriction is mediated by Rho kinase in vivo in human skin. Am J Physiol Heart Circ Physiol 292:H1700–H1705

    CAS  PubMed  Google Scholar 

  • Thorsson O, Lilja B, Ahlgren LARS, Hemdal BENGT, Westlin NILS (1985) The effect of local cold application on intramuscular blood flow at rest and after running. Med Sci Sports Exerc 17(6):710–713

    CAS  PubMed  Google Scholar 

  • Vaile J, O’Hagan C, Stefanovic B, Walker M, Gill N, Askew CD (2011) Effect of cold-water immersion on repeated cycling performance and limb blood flow. Br J Sports Med 45(10):825–829

    CAS  PubMed  Google Scholar 

  • Vallerand AL, Lupien J, Bukowiecki LJ (1983) Interactions of cold exposure and starvation on glucose tolerance and insulin response. Am J Physiol 245:E575–E581

    CAS  PubMed  Google Scholar 

  • Vallerand AL, Perusse F, Bukowiecki LJ (1987) Cold exposure potentiates the effect of insulin on in vivo glucose uptake. Am J Physiol 253:E179–E186

    CAS  PubMed  Google Scholar 

  • van Loon LJC, Greenhaff PL, Constantin-Teodosiu D, Saris WHM, Wagenmakers AJM (2001) The effects of increasing exercise intensity on muscle fuel utilisation in humans. J Physiol 536(1):295–304

    PubMed  PubMed Central  Google Scholar 

  • Wilson TE, Sauder CL, Kearney ML, Kuipers NT, Leuenberger UA, Monahan KD, Ray CS (2007) Skin-surface cooling elicits peripheral and visceral vasoconstriction in humans. J Appl Physiol 103:1257–1262

    PubMed  Google Scholar 

  • Yanagisawa O, Homma T, Okuwaki T, Shimao D, Takahashi H (2007) Effects of cooling on human skin and skeletal muscle. Eur J Appl Physiol 100:737–745

    PubMed  Google Scholar 

  • Zhang L, Vincent MA, Richards SM, Clerk LH, Rattigan S, Clark MG et al (2004) Insulin sensitivity of muscle capillary recruitment in vivo. Diabetes 53(2):447–453

    CAS  PubMed  Google Scholar 

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Acknowledgements

We want to thank all participants for taking part in this study. Dr. Gagnon is supported by a Natural Sciences and Engineering Research Council of Canada Discovery Grant (NSERC#2016-060883).

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Authors and Affiliations

  1. Laboratory of Environmental Exercise Physiology, School of Human Kinetics, Laurentian University, 935 Ramsey Lake Rd., Ben Avery Building, Sudbury, ON, P3E 2C6, Canada

    Dominique D. Gagnon, Curtis Hancock, Alexus McCue, Nicholas Beckett-Brown & Stephanie Munten

  2. Center of Research in Occupational Health and Safety, Laurentian University, Sudbury, ON, Canada

    Dominique D. Gagnon, Curtis Hancock, Alexus McCue, Nicholas Beckett-Brown & Stephanie Munten

  3. Department of Biology, Laurentian University, Sudbury, ON, Canada

    Jeffrey Gagnon & Laura Williams

  4. Northern Ontario School of Medicine, Sudbury, ON, Canada

    David Marsh

  5. Health Sciences North Research Institute, Sudbury, ON, Canada

    David Marsh

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  1. Dominique D. Gagnon
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  2. Curtis Hancock
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  3. Alexus McCue
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Contributions

All authors contributed to the study conception and design. Material preparation was performed by DDG, CH, AM, JG, and NB-B. Data collection DDG, CH, AM, DM, LW, SM, and NB-B. Data reduction and analysis were performed by DDG, LW, JG, and SM. The first draft of the manuscript was written by DDG and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Dominique D. Gagnon.

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The authors declare that they have no conflict of interest.

Ethical standards

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee (Laurentian University Research Ethics Board; LUREB #6014986) and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

Informed consent

All participants who took part in the present work provided written informed consent. Their data remained protected, confidential, and private.

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Communicated by George Havenith.

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Gagnon, D.D., Hancock, C., McCue, A. et al. Muscle cooling modulates tissue oxidative and biochemical responses but not energy metabolism during exercise. Eur J Appl Physiol 120, 1761–1775 (2020). https://doi.org/10.1007/s00421-020-04407-4

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