Skip to main content
Log in

The interactive effect of cooling and hypoxia on forearm fatigue development

  • Original Article
  • Published:
European Journal of Applied Physiology Aims and scope Submit manuscript

Abstract

Purpose

To examine the effect of separate and combined exposure to hypoxia [normoxia (FIO2 = 0.21) vs. moderate altitude (FIO2 = 0.13)] and temperature [thermoneutral (22 °C) vs. cold (5 °C)] on muscle fatigue development in the forearm, after repeated low-resistance contractions.

Methods

Eight males were exposed for 70 min to four separate conditions in a balanced order. Conditions were normoxic-thermoneutral (N), hypoxic-thermoneutral, normoxic-cold and hypoxic-cold. After 15-min seated rest, participants carried out intermittent dynamic forearm exercise at 15 % maximal isometric voluntary contraction (MVC) for eight consecutive, 5-min work bouts. Each bout was separated by 110 s rest during which MVC force was collected.

Results

When exposed to hypoxia and cold independently, the exercise protocol decreased MVC force of the finger flexors by 8.1 and 13.9 %, respectively, compared to thermoneutral normoxia. When hypoxia and cold were combined, the decrease in MVC force was 21.4 % more than thermoneutral normoxia, reflecting an additive effect and no interaction. EMG relative to force produced during MVC, increased by 2 and 1.2 μV per kg (36 and 23 % of N) for cold and hypoxia, respectively. When the stressors were combined the effect was additive, increasing to 3.1 μV per kg (56 % of N).

Conclusion

When compared to exercise in thermoneutral normoxic conditions, both cold and hypoxia significantly reduce brief MVC force output. This effect appears to be of mechanical origin, not a failure in muscle fibre recruitment per se. Additionally, the reduction in force is greater when the stressors are combined, showing an additive effect.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

ANOVA:

Analysis of variance

AU:

Arbitrary units

C:

Condition normoxic-cold

EMG:

Electromyography

ED:

Extensor digitorum

FCR:

Flexor carpi radialis

FDS:

Flexor digitorum superficialis

FFT:

Fast Fourier transform

FI:

Fatigue index

FIO2 :

Fraction of inspired oxygen

H:

Condition hypoxic-thermoneutrality

HC:

Conditions hypoxic-cold

HR:

Heart rate

LDF:

Laser Doppler flowmetry

MVC:

Maximal voluntary contraction

N:

Condition normoxic-thermoneutrality

RMS:

Root mean square

RPE:

Rate of perceived exertion

SpO2 :

Peripheral arterial oxygen saturation

Tco :

Core temperature

Ta :

Ambient temperature

Tsk :

Skin temperature

References

  • Allen DG, Lamb GD, Westerblad H (2008) Skeletal muscle fatigue: cellular mechanisms. Physiol Rev 88:287–332

    Article  CAS  PubMed  Google Scholar 

  • Amann M, Calbet JAL (2007) Convective oxygen transport and fatigue. J Appl Physiol 104:861–870

    Article  PubMed  Google Scholar 

  • Amann M, Dempsey JA (2007) Peripheral muscle fatigue from hyperoxia to moderate hypoxia—a carefully regulated variable? Physiology News 66:28–29

    Google Scholar 

  • Amann M, Eldridge MW, Lovering AT, Stickland MK, Pegelow DF, Dempsey JA (2006a) Arterial oxygenation influences central motor output and exercise performance via effects on peripheral locomotor muscle fatigue. J Physiol 575:937–952

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Amann M, Romer LM, Pegelow DF, Jacques AJ, Hess CJ, Dempsey JA (2006b) Effects of arterial oxygen content on peripheral locomotor muscle fatigue. J Appl Physiol 101:119–127

    Article  PubMed  Google Scholar 

  • Amann M, Pegelow DF, Jacques AJ, Dempsey JA (2007a) Inspiratory muscle work in acute hypoxia influences locomotor muscle fatigue and exercise performance of healthy humans. Am J Physiol Regul Integr Comp Physiol 293:R2036–R2045

    Article  CAS  PubMed  Google Scholar 

  • Amann M, Romer LM, Subudhi AW, Pegelow DF, Dempsey JA (2007b) Severity of arterial hypoxaemia affects the relative contributions of peripheral muscle fatigue to exercise performance in healthy humans. J Physiol 581:389–403

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Amann M, Venturelli M, Ives SJ, McDaniel J, Layec G, Rossman MJ, Richardson RS (2013) Peripheral fatigue limits endurance exercise via a sensory feedback-mediated reduction in spinal motoneuronal output. J Appl Physiol 115:355–364

    Article  PubMed Central  PubMed  Google Scholar 

  • Bergh U (1980) Human power at subnormal body temperatures. Acta Physiol Scand 478:1–39

    CAS  Google Scholar 

  • Bergh U, Ekblom B (1979a) Influence of muscle temperature on maximal muscle strength and power output in human skeletal muscles. Acta Physiol Scand 107:33–37

    Article  CAS  PubMed  Google Scholar 

  • Bergh U, Ekblom B (1979b) Physical performance and peak aerobic power at different body temperatures. J Appl Physiol 46:885–889

    CAS  PubMed  Google Scholar 

  • Bigland-Ritchie B, Donovan EF, Roussos CS (1981) Conduction velocity and EMG power spectrum changes in fatigue of sustained maximal efforts. J Appl Physiol 51:1300–1305

    CAS  PubMed  Google Scholar 

  • Blomstrand E, Bergh U, Essen-Gustavsson B, Ekblom B (1984) Influence of low muscle temperature on muscle metabolism during intense dynamic exercise. Acta Physiol Scand 120:229–236

    Article  CAS  PubMed  Google Scholar 

  • Cahill F, Kalmar JM, Pretorius T, Gardiner PF, Giesbrecht GG (2011) Whole-body hypothermia has central and peripheral influences on elbow flexor performance. Exp Physiol 96:528–538

    Article  PubMed  Google Scholar 

  • Cè E, Rampichini S, Agnello L, Limonta E, Veicsteinas A, Esposito F (2012) Combined effects of fatigue and temperature manipulation on skeletal muscle electrical and mechanical characteristics during isometric contraction. J Electromyogr Kinesiol 22(3):348–355

    Article  PubMed  Google Scholar 

  • Christian RJ, Bishop DJ, Billaut F, Girard O (2014a) Peripheral fatigue is not critically regulated during maximal, intermittent, dynamic leg extensions. J Appl Physiol 117:1063–1073

    Article  PubMed  Google Scholar 

  • Christian RJ, Bishop DJ, Billaut F, Girard O (2014b) The role of sense of effort on self-selected power output. Front Physiol 5:115

    PubMed Central  PubMed  Google Scholar 

  • Cipriano LF, Goldman RF (1975) Thermal responses of unclothed men exposed to both cold temperatures and high altitudes. J Appl Physiol 39:796–800

    CAS  PubMed  Google Scholar 

  • De Ruiter CJ, De Haan A (2000) Temperature effect on the force/velocity relationship of the fresh and fatigued human adductor pollicus muscle. Pflügers Arch 440:163–170

    Article  PubMed  Google Scholar 

  • Edwards R (1981) Human muscle function and fatigue. In: Porter R, Whelan J (eds) Human Muscle Fatigue Physiological Mechanisms. Pitman, London, pp 1–8

    Google Scholar 

  • Enoka RM, Stuart DG (1992) Neurobiology of muscle fatigue. J Appl Physiol 72:1631–1648

    Article  CAS  PubMed  Google Scholar 

  • Faulkner JA, Zerba E, Brooks SV (1990) Muscle temperature of mammals: cooling impairs most functional properties. Am J Physiol Regul Integr Comp Physiol 28:R259–R265

    Google Scholar 

  • Ferretti G (1992) Cold and muscle performance. Int J Sports Med 13(Suppl 1):185–187

    Article  Google Scholar 

  • Fitts RH (1994) Cellular mechanisms of muscle fatigue. Physiol Rev 74:49–94

    CAS  PubMed  Google Scholar 

  • Folt CL, Chen CY, Moore MV, Burnaford J (1999) Synergism and antagonism among multiple stressors. Limnol Oceanogr 44:864–877

    Article  Google Scholar 

  • Fulco CS, Cymerman A, Muza SR, Rock PB, Pandolf KB, Lewis SF (1994) Adductor pollicis muscle fatigue during acute and chronic altitude exposure and return to sea level. J Appl Physiol 77:179–183

    CAS  PubMed  Google Scholar 

  • Fulco CS, Lewis SF, Frykman PN, Boushel R, Smith S, Harman EA, Cymerman A, Pandolf KB (1996) Muscle fatigue and exhaustion during dynamic leg exercise in normoxia and hypobaric hypoxia. J Appl Physiol 81:1891–1900

    CAS  PubMed  Google Scholar 

  • Gandevia SC (2001) Spinal and supraspinal factors in human muscle fatigue. Physiol Rev 81:1725–1789

    CAS  PubMed  Google Scholar 

  • Gaoua N, Grantham J, El Massioui F, Girard O, Racinais S (2011) Cognitive decrements do not follow neuromuscular alterations during passive heat exposure. Int J Hyperthermia 27:10–19

    Article  PubMed  Google Scholar 

  • Gautier H, Bonora M, Schultz SA, Remmers JE (1987) Hypoxia-induced changes in shivering and body temperature. J Appl Physiol 62:2477–2484

    CAS  PubMed  Google Scholar 

  • Goodall S, Ross EZ, Romer LM (2010) Effect of graded hypoxia on supraspinal contributions to fatigue with unilateral knee-extensor contractions. J Appl Physiol 109:1842–1851

    Article  PubMed  Google Scholar 

  • Gregson W, Black MA, Jones H, Milson J, Morton J, Dawson B, Atkinson G, Green D (2011) Influence of cold water immersion on limb and cutaneous blood flow at rest. Am J Sports Med 39(6):1316–1323

    Article  PubMed  Google Scholar 

  • Haseler LJ, Hogan MC, Richardson RS (1999) Skeletal muscle phosphocreatine recovery in exercise-trained humans is dependent on O2 availability. J Appl Physiol 86:2013–2018

    CAS  PubMed  Google Scholar 

  • Hermens HJ, Freriks B, Disselhorst-Klug C, Rau G (2000) Development of recommendations for SEMG sensors and sensor placement procedures. J Electromyogr Kinesiol 10:361–374

    Article  CAS  PubMed  Google Scholar 

  • Hogan MC, Richardson RS, Haseler LJ (1999) Human muscle performance and PCr hydrolysis with varied inspired oxygen fractions: a 31P-MRS study. J Appl Physiol 86:1367–1373

    CAS  PubMed  Google Scholar 

  • Johnston CE, White MD, Wu M, Bristow GK, Giesbrecht GG (1996) Eucapnic hypoxia lowers human cold thermoregulatory response thresholds and accelerates core cooling. J Appl Physiol 80:422–429

    CAS  PubMed  Google Scholar 

  • Katayama K, Amann M, Pegelow DF, Jacques AJ, Dempsey JA (2007) Effect of arterial oxygenation on quadriceps fatigability during isolated muscle exercise. Am J Physiol Regul Integr Comp Physiol 292:R1279–R1286

    Article  CAS  PubMed  Google Scholar 

  • Kossler F, Lange F, Kuchler G (1987) Isometric twitch and tetanic contraction of frog skeletal muscles at temperatures between 0 to 30°C. Biomed Biochim Acta 46:809–814

    CAS  PubMed  Google Scholar 

  • Lloyd A, Hodder S, Faulkner S, Fry A, Havenith G (2014) Muscle temperature limits isometric endurance via sensory feedback-mediated central fatigue. Med Sci Sports Exerc 46(5S):180–187

    Google Scholar 

  • Marcora SM, Staiano W (2010) The limit to exercise tolerance in humans: mind over muscle? Eur J Appl Physiol 109(4):763–770

    Article  PubMed  Google Scholar 

  • McArdle WD, Magel JR, Lesmes GR, Pechar GS (1976) Metabolic and cardiovascular adjustment to work in air and water at 18, 25, and 33°C. J Appl Physiol 40(l):85–90

    CAS  PubMed  Google Scholar 

  • Millet GY, Aubert D, Favier FB, Busso T, Benoît H (2008) Effect of acute hypoxia on central fatigue during repeated isometric leg contractions. Scand J Med Sci Sports 19:695–702

    Article  PubMed  Google Scholar 

  • Millet GY, Muthalib M, Jubeau M, Laursen PB, Nosaka K (2012) Severe hypoxia affects exercise performance independently of afferent feedback and peripheral fatigue. J Appl Physiol 112:1335–1344

    Article  PubMed  Google Scholar 

  • Moor Instruments (2004) MoorLab laser Doppler blood flow user manual

  • Mucke R, Heuer D (1989) Behaviour of EMG parameters and conduction velocity in contractions with different muscle temperatures. Biomed Bichim Acta 5(6):459–464

    Google Scholar 

  • Oksa J, Rintamäki H, Rissanen S (1997) Muscle performance and electromyographic activity of the lower leg muscles with different levels of cold exposure. Eur J Appl Physiol 75:484–490

    Article  CAS  Google Scholar 

  • Oksa J, Ducharme M, Rintamäki H (2002) Combined effect of repetitive work and cold on muscle function and fatigue. J Appl Physiol 92:354–361

    PubMed  Google Scholar 

  • Perrey S, Rupp T (2009) Altitude-induced changes in muscle contractile properties. High Alt Med Biol 10:175–182

    Article  CAS  PubMed  Google Scholar 

  • Racinais S (2013) Hot ambient conditions shift the Force/EMG relationship. Springerplus 2:317

    Article  PubMed Central  PubMed  Google Scholar 

  • Racinais S, Oksa J (2010) Temperature and neuromuscular function. Scand J Med Sci Sports 20:1–18

    Article  PubMed  Google Scholar 

  • Ray CA, Hume KM, Gracey KH, Mahoney ET (1997) Muscle cooling delays activation of the muscle metaboreflex in humans. Am J Physiol Heart Circ Physiol 273:2436–2441

    Google Scholar 

  • Robinson KA, Haymes EM (1990) Metabolic effects of exposure to hypoxia plus cold at rest and during exercise in humans. J Appl Physiol 68:720–725

    CAS  PubMed  Google Scholar 

  • Segal SS, Faulkner JA, White TP (1986) Skeletal muscle fatigue in vitro is temperature dependent. J Appl Physiol 61:660–665

    CAS  PubMed  Google Scholar 

  • Simmons GH, Fieger SM, Minson CT, Halliwill JR (2010) Hypoxic cutaneous vasodilation is sustained during brief cold stress and is not affected by changes in CO2. J Appl Physiol 108:788–792

    Article  PubMed  Google Scholar 

  • Simmons GH, Barrett-O’Keefe Z, Minson CT, Halliwill JR (2011) Cutaneous vascular and core temperature responses to sustained cold exposure in hypoxia. Exp Physiol 96:1062–1071

    Article  PubMed  Google Scholar 

  • Sweitzer N, Moss R (1990) The effect of altered temperature on Ca2 + -sensitive force in permeabilized myocardium and skeletal muscles. J Gen Physiol 96:1221–1245

    Article  CAS  PubMed  Google Scholar 

  • Thompson CS, Holowatz LA, Kenney WL (2005) Cutaneous vasoconstrictor responses to norepinephrine are attenuated in older humans. Am J Physiol Regul Integr Comp Physiol 288:R1108–R1113

    Article  CAS  PubMed  Google Scholar 

  • Tipton M (2012) A case for combined environmental stressor studies. Extrem Physiol Med 1:7–8

    Article  PubMed Central  PubMed  Google Scholar 

  • Todd G, Butler JE, Taylor JL, Gandevia SC (2005) Hyperthermia: a failure of the motor cortex and the muscle. J Physiol 563:621–631

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • West W, Hicks A, Clements L, Downing J (1995) The relationship between voluntary electromyogram, endurance time and intensity of effort in isometric handgrip exercise. Eur J Appl Physiol 71(301):30

    Google Scholar 

  • Wood SC (1991) Interactions between hypoxia and hypothermia. Annu Rev Physiol 53:71–85

    Article  CAS  PubMed  Google Scholar 

  • Yanagisawa O, Kudo H, Takahashi N, Yoshioka H (2004) Magnetic resonance imaging evaluation of cooling on blood flow and oedema in skeletal muscles after exercise. Eur J Appl Physiol 91:737–740

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to George Havenith.

Additional information

Communicated by Nicolas Place.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lloyd, A., Hodder, S. & Havenith, G. The interactive effect of cooling and hypoxia on forearm fatigue development. Eur J Appl Physiol 115, 2007–2018 (2015). https://doi.org/10.1007/s00421-015-3181-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00421-015-3181-1

Keywords

Navigation