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The influence of a mild thermal challenge and severe hypoxia on exercise performance and serum BDNF

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Abstract

Aim

To examine the isolated and combined effects of severe hypoxia and a mild thermal challenge on performance, physiological measures, cognition, and serum brain-derived neurotrophic factor (BDNF).

Methods

Nine trained male athletes (age: 23 ± 3 years; W max: 333 ± 45 W) completed four experimental trials (CON: 15 °C/0 m, ALT: 15 °C/3800 m, TEMP: 25 °C/0 m, ALT + TEMP: 25 °C/3800 m) in a double blind, randomized, cross-over design. Subjects cycled for 30 min in a self-paced test starting at 75 % W max, their goal was to ‘perform as much work as possible in 30 min.’ Power output, heart rate, blood lactate, pulse oximetry, core and skin temperature, thermal sensation, ratings of perceived exertion, reaction time (RT), and BDNF were assessed.

Results

The amount of work produced in 30 min was reduced by temperature (F(1,8) = 7.1; p = 0.029; 360 ± 19 kJ in 15 °C; 344 ± 18 kJ in 25 °C) and altitude (F(1,8) = 94.2; p < 0.001; 427 ± 24 kJ at sea level; 277 ± 15 kJ at altitude), yet there was no interaction effect. Altitude increased mean RT (F(1,8) = 8.0; p = 0.022; 281.9 ± 9.4 ms at sea level; 289.3 ± 10.0 ms at altitude) and RT variability (F(1,8) = 8.5; p = 0.020; 44 ± 3 ms at sea level: 50 ± 4 ms at altitude). Exercise increased BDNF (F(1,8) = 15.2; p = 0.005; PRE: 21.8 ± 1.3 ng/mL; POST: 26.5 ± 2.1 ng/mL).

Conclusion

Exercise capacity was significantly reduced due to an increase in altitude (3800 m; −34.3 %) or a 10 °C increase in ambient temperature (−3.2 %). The combination of both stressors showed to be additive (−38.0 %). Altitude induced an increase in RT and RT variability presenting a deterioration in cognitive functioning during acute hypoxia. Exercise significantly increased BDNF, but no effect of altitude on the BDNF concentration was observed.

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Abbreviations

A:

Acclimation

ANOVA:

Analysis of variance

BDNF:

Serum brain-derived neurotrophic factor

Bla:

Blood lactate

BBB:

Blood brain barrier

Bpm:

Beats per minute

HR:

Heart rate

PVT:

Psychomotor vigilance task

RPE:

Rating of perceived exertion

RT:

Reaction time

s:

Seconds

SaO2 :

Arterial hemoglobin oxygen saturation

R:

Recovery

T core :

Core temperature

TMS:

Transcranial magnetic stimulation

Tsens:

Thermal sensation

T skin :

Skin temperature

TT:

Time trial

VO2max:

Maximal oxygen uptake

W:

Watt

W max :

Maximal exercise ability

W out :

Workload of the last completed stage

WU:

Warm-up

References

  • Acheson A, Conover JC, Fandl JP, Dechiara TM, Russell M, Thadani A, Squinto SP, Yancopoulos GD, Lindsay RM (1995) A BDNF autocrine loop in adult sensory neurons prevents cell death. Nature 374:450–453

    Article  CAS  PubMed  Google Scholar 

  • Amann M, Calbet JA (2008) Convective oxygen transport and fatigue. J Appl Physiol 104:861–870

    Article  PubMed  Google Scholar 

  • Amann M, Romer LM, Pegelow DF, Jacques AJ, Hess CJ, Dempsey JA (2006) Effects of arterial oxygen content on peripheral locomotor muscle fatigue. J Appl Physiol (1985) 101(1):119–127

    Article  Google Scholar 

  • Bartsch P, Pfluger N, Audetat M, Shaw S, Weidmann P, Vock P, Vetter W, Rennie D, Oelz O (1991) Effects of slow ascent to 4559 M on fluid homeostasis. Aviat Space Environ Med 62:105–110

    CAS  PubMed  Google Scholar 

  • Beidleman BA, Fulco CS, Staab JE, Andrew SP, Muza SR (2014) Cycling performance decrement is greater in hypobaric versus normobaric hypoxia. Extrem Physiol Med 3:8

    Article  PubMed Central  PubMed  Google Scholar 

  • Bishop B, Silva G, Krasney J, Salloum A, Roberts A, Nakano H, Shucard D, Rifkin D, Farkas G (2000) Circadian rhythms of body temperature and activity levels during 63 h of hypoxia in the rat. Am J Physiol Regul Integr Comp Physiol 279:R1378–R1385

    CAS  PubMed  Google Scholar 

  • Bjursten H, Ederoth P, Sigurdsson E, Gottfredsson M, Syk I, Einarsson O, Gudbjartsson T (2010) S100B profiles and cognitive function at high altitude. High Alt Med Biol 11(1):31–38

    Article  CAS  PubMed  Google Scholar 

  • Borg GA (1982) Psychophysical bases of perceived exertion. Med Sci Sports Exerc 14:377–381

    CAS  PubMed  Google Scholar 

  • Buchheit M, Simpson BM, Garvican-lewis LA, Hammond K, Kley M, Schmidt WF, Aughey RJ, Soria R, Sargent C, Roach GD, Claros JC, Wachsmuth N, Gore CJ, Bourdon PC (2013) Wellness, fatigue and physical performance acclimatisation to a 2-week soccer camp at 3600 m (ISA3600). Br J Sports Med 47(Suppl 1):i100–i106

    Article  PubMed Central  PubMed  Google Scholar 

  • Cadena V, Tattersall GJ (2014) Body temperature regulation during acclimation to cold and hypoxia in rats. J Therm Biol 46:56–64

    Article  CAS  PubMed  Google Scholar 

  • De Pauw K, Roelands B, Cheung SS, De Geus B, Rietjens G, Meeusen R (2013a) Guidelines to classify subject groups in sport-science research. Int J Sports Physiol Perform 8:111–122

    PubMed  Google Scholar 

  • De Pauw K, Roelands B, Marusic U, Tellez HF, Knaepen K, Meeusen R (2013b) Brain mapping after prolonged cycling and during recovery in the heat. J Appl Physiol (1985) 115(9):1324–1331

    Article  Google Scholar 

  • DiPasquale DM, Kolkhorst FW, Buono MJ (2015) Acute normobaric hypoxia reduces body temperature in humans. High Alt Med Biol 16(1):61–66

    Article  CAS  PubMed  Google Scholar 

  • Engelhardt S, Patkar S, Ogunshola OO (2014) Cell-specific blood-brain barrier regulation in health and disease: a focus on hypoxia. Br J Pharmacol 171(5):1210–1230

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ferris LT, Williams JS, Shen CL (2007) The effect of acute exercise on serum brain-derived neurotrophic factor levels and cognitive function. Med Sci Sports Exerc 39(4):728–734

    Article  CAS  PubMed  Google Scholar 

  • Galloway SD, Maughan RJ (1997) Effects of ambient temperature on the capacity to perform prolonged cycle exercise in man. Med Sci Sports Exerc 29:1240–1249

    Article  CAS  PubMed  Google Scholar 

  • Gavhed DC, Holmér I (1996) Physiological and subjective responses to thermal transients of exercising subjects dressed in cold-protective clothing. Eur J Appl Physiol Occup Physiol 73(6):573–581

    Article  CAS  PubMed  Google Scholar 

  • Girard O, Racinais S (2014) Combining heat stress and moderate hypoxia reduces cycling time to exhaustion without modifying neuromuscular fatigue characteristics. Eur J Appl Physiol 114:1521–1532

    Article  PubMed Central  PubMed  Google Scholar 

  • Goekint M, Roelands B, Heyman E, Njemini R, Meeusen R (2011) Influence of citalopram and environmental temperature on exercise-induced changes in BDNF. Neurosci Lett 494(2):150–154

    Article  CAS  PubMed  Google Scholar 

  • Gold SM, Schulz KH, Hartmann S, Mladek M, Lang UE, Hellweg R, Reer R, Braumann KM, Heesen C (2003) Basal serum levels and reactivity of nerve growth factor and brain-derived neurotrophic factor to standardized acute exercise in multiple sclerosis and controls. J Neuroimmunol 138(1–2):99–105

    Article  CAS  PubMed  Google Scholar 

  • Goodall S, Twomey R, Amann M (2014) Acute and chronic hypoxia: implications for cerebral function and exercise tolerance. Fatigue 2:73–92

    PubMed Central  PubMed  Google Scholar 

  • Griffin ÉW, Mullally S, Foley C, Warmington SA, O’Mara SM, Kelly AM (2011) Aerobic exercise improves hippocampal function and increases BDNF in the serum of young adult males. Physiol Behav 104(5):934–941

    Article  CAS  PubMed  Google Scholar 

  • Grishin OV (2011) Adaptive hypometabolism in man. Vestn Ross Akad Med Nauk 8:33–41

    PubMed  Google Scholar 

  • Ha M, Tokura H, Gotoh J, Holmér I (1998) Effects of two kinds of underwear on metabolic heat production during 60 min recovery after 30 min severe exercise in the cold. Appl Human Sci 17(5):173–179

    Article  CAS  PubMed  Google Scholar 

  • Helan M, Aravamudan B, Hartman WR, Thompson MA, Johnson BD, Pabelick CM, Prakash YS (2014) BDNF secretion by human pulmonary artery endothelial cells in response to hypoxia. J Mol Cell Cardiol 68:89–97

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hubold C, Lang UE, Gehring H, Schultes B, Schweiger U, Peters A, Hellweg R, Oltmanns KM (2009) Increased serum brain-derived neurotrophic factor protein upon hypoxia in healthy young men. J Neural Transm 116(10):1221–1225

    Article  CAS  PubMed  Google Scholar 

  • Julian CG, Subudhi AW, Wilson MJ, Dimmen AC, Pecha T, Roach RC (2011) Acute mountain sickness, inflammation, and permeability: new insights from a blood biomarker study. J Appl Physiol (1985) 111(2):392–399

    Article  CAS  Google Scholar 

  • Klass M, Roelands B, Lévénez M, Fontenelle V, Pattyn N, Meeusen R, Duchateau J (2012) Effects of noradrenaline and dopamine on supraspinal fatigue in well-trained men. Med Sci Sports Exerc 44(12):2299–2308

    Article  CAS  PubMed  Google Scholar 

  • Knaepen K, Goekint M, Heyman EM, Meeusen R (2010) Neuroplasticity—exercise-induced response of peripheral brain-derived neurotrophic factor: a systematic review of experimental studies in human subjects. Sports Med 40:765–801

    Article  PubMed  Google Scholar 

  • Knicker AJ, Renshaw I, Oldham AR, Cairns SP (2011) Interactive processes link the multiple symptoms of fatigue in sport competition. Sports Med 41:307–328

    Article  PubMed  Google Scholar 

  • Kobrick JL, Dusek ER (1970) Effects of hypoxia on voluntary response time to peripherally located visual stimuli. J Appl Physiol 29:444–448

    CAS  PubMed  Google Scholar 

  • Li P, Zhang G, You HY, Zheng R, Gao YQ (2012) Training-dependent cognitive advantage is suppressed at high altitude. Physiol Behav 106(4):439–445

    Article  CAS  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Luks AM, Swenson ER (2011) Pulse oximetry at high altitude. High Alt Med Biol 12:109–119

    Article  PubMed  Google Scholar 

  • Marino FE (2012) The limitations of the constant load and self-paced exercise models of exercise physiology. Comp Exerc Physiol 7:173–178

    Article  Google Scholar 

  • Mortola JP, Seifert EL (2000) Hypoxic depression of circadian rhythms in adult rats. J Appl Physiol (1985) 2:365–368

    Google Scholar 

  • Natah SS, Srinivasan S, Pittman Q, Zhao Z, Dunn JF (2009) Effects of acute hypoxia and hyperthermia on the permeability of the blood-brain barrier in adult rats. J Appl Physiol (1985) 107(4):1348–1356

    Article  PubMed Central  CAS  Google Scholar 

  • Ogunshola OO, Al-Ahmad A (2012) HIF-1 at the blood-brain barrier: a mediator of permeability? High Alt Med Biol 13(3):153–161

    Article  CAS  PubMed  Google Scholar 

  • Parkin JM, Carey MF, Zhao S, Febbraio MA (1999) Effect of ambient temperature on human skeletal muscle metabolism during fatiguing submaximal exercise. J Appl Physiol 86:902–908

    Article  CAS  PubMed  Google Scholar 

  • Parsons KC (2003) Human thermal environments. Taylor & Francis, London

    Google Scholar 

  • Périard JD, Cramer MN, Chapman PG, Caillaud C, Thompson MW (2011) Cardiovascular strain impairs prolonged self-paced exercise in the heat. Exp Physiol 96(2):134–144

    Article  PubMed  Google Scholar 

  • Périard JD, Thompson MW, Caillaud C, Quaresima V (2013) Influence of heat stress and exercise intensity on vastus lateralis muscle and prefrontal cortex oxygenation. Eur J Appl Physiol 113:211–222

    Article  PubMed  Google Scholar 

  • Pilcher JJ, Nadler E, Busch C (2002) Effects of hot and cold temperature exposure on performance: a meta-analytic review. J Appl Physiol 113:211–222

    Google Scholar 

  • Ramanathan NL (1964) A new weighting system for mean surface temperature of the human body. J Appl Physiol 19:531–533

    CAS  PubMed  Google Scholar 

  • Rite I, Machado A, Cano J, Venero JL (2007) Blood–brain barrier disruption induces in vivo degeneration of nigral dopaminergic neurons. J Neurochem 101:1567–1582

    Article  CAS  PubMed  Google Scholar 

  • Roelands B, Meeusen R (2010) Alterations in central fatigue by pharmacological manipulations of neurotransmitters in normal and high ambient temperature. Sports Med 40:229–246

    Article  PubMed  Google Scholar 

  • Roelands B, De Koning J, Foster C, Hettinga F, Meeusen R (2013) Neurophysiological determinants of theoretical concepts and mechanisms involved in pacing. Sports Med 43(5):301–311

    Article  PubMed  Google Scholar 

  • Steiner AA, Branco LG (2002) Hypoxia-induced anapyrexia: implications and putative mediators. Annu Rev Physiol 64:263–288

    Article  CAS  PubMed  Google Scholar 

  • Tatterson AJ, Hahn AG, Martin DT, Febbraio MA (2000) Effects of heat stress on physiological responses and exercise performance in elite cyclists. J Sci Med Sport 3(2):186–193

    Article  CAS  PubMed  Google Scholar 

  • Verges S, Rupp T, Jubeau M, Wuyam B, Esteve F, Levy P, Perrey S, Millet GY (2012) Cerebral perturbations during exercise in hypoxia. Am J Physiol Regul Integr Comp Physiol 302:R903–R916

    Article  CAS  PubMed  Google Scholar 

  • Vogiatzis I, Louvaris Z, Habazettl H, Athanasopoulos D, Andrianopoulos V, Cherouveim E, Wagner H, Roussos C, Wagner PD, Zakynthinos S (2011) Frontal cerebral cortex blood flow, oxygen delivery and oxygenation during normoxic and hypoxic exercise in athletes. J Physiol 589:4027–4039

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Watson P, Shirreffs S, Maughan R (2005) Blood–brain barrier integrity may be threatened by exercise in a warm environment. Am J Physiol Regul Integr Comp Physiol 288:R1689–R1694

    Article  CAS  PubMed  Google Scholar 

  • Wood SC (1995) Interrelationships between hypoxia and thermoregulation in vertebrates. Adv Comp Environ Physiol 22:209–231

    Article  Google Scholar 

  • Wu XY, Li XY, Wang JT, Zhuang Y, Du JY (2002) Effects of simulated high altitude hypoxia on cognitive performance. Zhongguo Ying Yong Sheng Li Xue Za Zhi 18(1):34–37

    PubMed  Google Scholar 

  • Zlokovic B (2008) The blood-brain barrier in health and chronic neurodegenerative disorders. Neuron 57:178–201

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

Bart Roelands is a post-doctoral fellow of the Fund for Scientific Research. We thank the Military Hospital Queen Astrid for the use of their infrastructure and personnel. We thank Matthias Verstraelen, Jennifer Bal, Maxime Tuerlinckx, and our subjects for their hard work during the experimental test period.

Conflicts of interest

No conflicts of interest, financial or otherwise, are declared by the author(s).

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Correspondence to Bart Roelands.

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Communicated by George Havenith.

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Van Cutsem, J., Pattyn, N., Vissenaeken, D. et al. The influence of a mild thermal challenge and severe hypoxia on exercise performance and serum BDNF. Eur J Appl Physiol 115, 2135–2148 (2015). https://doi.org/10.1007/s00421-015-3193-x

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