Subscribe to RSS
DOI: 10.1055/a-2647-2236
Hypoxia Impairs Neuromuscular Function More Than Heat After Incremental Test to Exhaustion
Supported by: Science and Technology Innovation Plan Of Shanghai Science and Technology Commission 22dz1204601

Abstract
Heat stress and hypoxia impair athletic performance through inflammation, muscle injury, and neuromuscular dysfunction. This study examined these effects in 15 endurance athletes (13 males and 2 females, VO2max=59.5±3.9 ml/min/kg) performing incremental load tests to exhaustion under normal (CON), hypoxic (HYP), and high-temperature and humidity (HOT) conditions. Pre- and postexercise assessments, including blood biomarkers, performance, and surface electromyography (sEMG) during the counter-movement jump (CMJ) and isometric mid-thigh pull (IMTP), were conducted under normal conditions. Compared to CON, time to exhaustion was significantly reduced in HYP and HOT (p<0.05). CMJ performance declined under CON and HYP (p<0.05). Force at 200 and 250 ms decreased under both CON and HYP during IMTP (p<0.05). The root mean square (RMS) and the median power frequency (MPF) were decreased under HYP during CMJ and IMTP (p<0.05). In contrast, no significant differences in sEMG and kinetic markers were observed in the HOT (p>0.05). No significant changes in creatine kinase and lactate dehydrogenase levels were observed (p>0.05). Postexercise, tumor necrosis factor-alpha was lower in HYP (p<0.05), while interleukin-6 increased in HOT (p<0.05). Hypoxia impairs neuromuscular function and suppresses inflammation, whereas heat stress induces inflammation without neuromuscular deficits.
Keywords
acute environmental stressors - inflammatory cytokines - neuromuscular fatigue - electromyographic analysis - biomechanical assessmentPublication History
Received: 14 November 2024
Accepted after revision: 01 July 2025
Accepted Manuscript online:
01 July 2025
Article published online:
05 September 2025
© 2025. Thieme. All rights reserved.
Georg Thieme Verlag KG
Oswald-Hesse-Straße 50, 70469 Stuttgart, Germany
-
References
- 1
Osawa T,
Arimitsu T,
Takahashi H.
Hypoxia affects tissue oxygenation differently in the thigh and calf muscles
during incremental running. Eur J Appl Physiol 2017; 117: 2057-2064
MissingFormLabel
- 2
Jung W-S,
Kim S-W,
Park H-Y,
Kim J,
Lim K.
Effects of acute exposure to thermal stress on cardiorespiratory function,
skeletal muscle oxygenation, and exercise performance in healthy males. Int J Environ
Res Public Health 2021; 18: 7404
MissingFormLabel
- 3
Fortney SM,
Vroman NB.
Exercise, performance and temperature control: temperature regulation during
exercise and implications for sports performance and training. Sports Med 1985; 2:
8-20
MissingFormLabel
- 4
No M,
Kwak H-B.
Effects of environmental temperature on physiological responses during
submaximal and maximal exercises in soccer players. Integr Med Res 2016; 5: 216-222
MissingFormLabel
- 5
Ely MR,
Cheuvront SN,
Roberts WO,
Montain SJ.
Impact of weather on marathon-running performance. Med Sci Sports Exerc 2007; 39:
487-493
MissingFormLabel
- 6
Ušaj A,
Mekjavic IB,
Kapus J,
McDonnell AC,
Jaki Mekjavic P,
Debevec T.
Muscle oxygenation during hypoxic exercise in children and adults. Front Physiol 2019;
10: 1385
MissingFormLabel
- 7
Takezawa T,
Dobashi S,
Koyama K.
Cardiorespiratory response and power output during submaximal exercise in
normobaric versus hypobaric hypoxia: a pilot study using a specific chamber that
controls environmental factors. High Alt Med Biol 2021; 22: 201-208
MissingFormLabel
- 8
Tidball JG.
Mechanisms of muscle injury, repair, and regeneration. Compr Physiol 2011; 1: 2029-2062
MissingFormLabel
- 9
Pedersen BK,
Hoffman-Goetz L.
Exercise and the immune system: regulation, integration, and adaptation. Physiol Rev
2000; 80: 1055-1081
MissingFormLabel
- 10
Gutiérrez-Vargas R,
Martín-Rodríguez S,
Sánchez-Ureña B.
et al.
Biochemical and muscle mechanical postmarathon changes in hot and humid
conditions. J Strength Cond Res 2020; 34: 847-856
MissingFormLabel
- 11
Lira FS,
Lemos VA,
Bittar IG.
et al.
Physiological and cytokine response to acute exercise under hypoxic conditions:
a pilot study. J Sports Med Phys Fit 2016; 57: 461-468
MissingFormLabel
- 12
Enoka RM,
Duchateau J.
Muscle fatigue: what, why and how it influences muscle function. J Physiol 2008; 586:
11-23
MissingFormLabel
- 13
Rodrigues JFC,
Mendes TT,
Gomes PF.
et al.
Reduced running performance and greater perceived exertion, but similar
post-exercise neuromuscular fatigue in tropical natives subjected to a 10 km
self-paced run in a hot compared to a temperate environment. PLoS One 2023; 18: e0290081
MissingFormLabel
- 14
Ftaiti F,
Kacem A,
Latiri I.
et al.
Comparison of male and female thermal, cardiac, and muscular responses induced
by a prolonged run undertaken in a hot environment. Can J Appl Physiol 2005; 30: 404-418
MissingFormLabel
- 15
McKeown DJ,
McNeil CJ,
Simmonds MJ,
Kavanagh JJ.
Post-fatigue ability to activate muscle is compromised across a wide range of
torques during acute hypoxic exposure. Eur J Neurosci 2022; 56: 4653-4668
MissingFormLabel
- 16
Scott BR,
Slattery KM,
Sculley DV.
et al.
Acute physiological responses to moderate-load resistance exercise in
hypoxia. J Strength Cond Res 2017; 31: 1973-1981
MissingFormLabel
- 17
Ball D.
Contrasting effects of heat stress on neuromuscular performance. Exp Physiol 2021;
106: 2328-2334
MissingFormLabel
- 18
Geng Z,
Wang J,
Cao G,
Tan C,
Li L,
Qiu J.
Differential impact of heat and hypoxia on dynamic oxygen uptake and
deoxyhemoglobin parameters during incremental exhaustive exercise. Front Physiol 2024;
14: 1247659
MissingFormLabel
- 19
Armstrong LE,
Maresh CM,
Castellani JW.
et al.
Urinary indices of hydration status. Int J Sport Nutr Exerc Metab 1994; 4: 265-279
MissingFormLabel
- 20
Yatsutani H,
Mori H,
Ito H,
Hayashi N,
Girard O,
Goto K.
Endocrine and metabolic responses to endurance exercise under hot and hypoxic
conditions. Front Physiol 2020; 11: 932
MissingFormLabel
- 21
Subudhi AW,
Dimmen AC,
Roach RC.
Effects of acute hypoxia on cerebral and muscle oxygenation during incremental
exercise. J Appl Physiol 2007; 103: 177-183
MissingFormLabel
- 22
Tan C,
Wang J,
Cao G.
et al.
Psychological changes in athletes infected with Omicron after
return to training: fatigue, sleep, and
mood. PeerJ 2023; 11: e15580
MissingFormLabel
- 23
Kang KT,
Koh YG,
Nam JH,
Jung M,
Kim SJ,
Kim SH.
Biomechanical evaluation of the influence of posterolateral corner structures on
cruciate ligaments forces during simulated gait and squatting. PLoS One 2019; 14:
e0214496
MissingFormLabel
- 24
Secomb JL,
Farley OR,
Lundgren L.
et al.
Associations between the performance of scoring manoeuvres and lower-body
strength and power in elite surfers. Int |J Sports Sci Coach 2015; 10: 911-918
MissingFormLabel
- 25
Liu Y,
Peng C-H,
Wei S-H,
Chi JC,
Tsai FR,
Chen JY.
Active leg stiffness and energy stored in the muscles during maximal counter
movement jump in the aged. J Electromyogr Kinesiol 2006; 16: 342-351
MissingFormLabel
- 26
Comfort P,
Dos’ Santos T,
Beckham GK.
et al.
Standardization and methodological considerations for the isometric midthigh
pull. Strength Cond J 2019; 41: 57-79
MissingFormLabel
- 27
Begalle RL,
DiStefano LJ,
Blackburn T,
Padua DA.
Quadriceps and hamstrings coactivation during common therapeutic exercises. J Athl
Train 2012; 47: 396-405
MissingFormLabel
- 28
Martinez SC,
Coons JM,
Mehls KD.
Effect of external load on muscle activation during the barbell
back squat. Eur J Sport Sci 2023; 23: 975-982
MissingFormLabel
- 29
Cohen J.
Statistical power analysis for the behavioral sciences. Routledge; 2013
MissingFormLabel
- 30
Soo J,
Racinais S,
Fairchild TJ,
Ihsan M,
Buchheit M,
Girard O.
Effects of graded hypoxia during exhaustive intermittent cycling on subsequent
exercise performance and neuromuscular responses. Eur J Appl Physiol 2021; 121: 3539-3549
MissingFormLabel
- 31
Silva RPM,
Barros CLM,
Mendes TT.
et al.
The influence of a hot environment on physiological stress responses in exercise
until exhaustion. PLoS One 2019; 14: e0209510
MissingFormLabel
- 32
Arngrímsson S,
Petitt D,
Borrani F,
Skinner K,
Cureton K.
Hyperthermia and maximal oxygen uptake in men and
women. Eur J Appl Physiol 2004; 92: 524-532
MissingFormLabel
- 33
Cheuvront SN,
Kenefick RW,
Montain SJ,
Sawka MN.
Mechanisms of aerobic performance impairment with heat stress and
dehydration. J Appl Physiol 2010; 109: 1989-1995
MissingFormLabel
- 34
Trinity JD,
Pahnke MD,
Lee JF,
Coyle EF.
Interaction of hyperthermia and heart rate on stroke volume during prolonged
exercise. J Appl Physiol 2010; 109: 745-751
MissingFormLabel
- 35
Amann M,
Romer LM,
Subudhi AW,
Pegelow DF,
Dempsey JA.
Severity of arterial hypoxaemia affects the relative contributions of peripheral
muscle fatigue to exercise performance in healthy humans. J Physiol 2007; 581: 389-403
MissingFormLabel
- 36
Boukhris O,
Trabelsi K,
Abdessalem R.
et al.
Effects of the 5-m shuttle run test on markers of muscle damage, inflammation,
and fatigue in healthy male athletes. Int J Environ Res Public Health 2020; 17: 4375
MissingFormLabel
- 37
Dupuy O,
Douzi W,
Theurot D,
Bosquet L,
Dugué B.
An evidence-based approach for choosing post-exercise recovery techniques to
reduce markers of muscle damage, soreness, fatigue, and inflammation: a
systematic review with meta-analysis. Front Physiol 2018; 9: 403
MissingFormLabel
- 38
Woo J,
Min J-H,
Lee Y-H,
Roh HT.
Effects of hyperbaric oxygen therapy on inflammation, oxidative/antioxidant
balance, and muscle damage after acute exercise in normobaric, normoxic and
hypobaric, hypoxic environments: a pilot study. Int J Environ Res Public Health 2020;
17: 7377
MissingFormLabel
- 39
Kasai N,
Kojima C,
Sumi D,
Ikutomo A,
Goto K.
Inflammatory, oxidative stress, and angiogenic growth factor responses to
repeated-sprint exercise in hypoxia. Front Physiol 2019; 10: 844
MissingFormLabel
- 40
Nybo L,
Nielsen B,
Klarlund Pedersen B,
Møller K,
Secher NH.
Interleukin-6 release from the human brain during prolonged exercise. J Physiol 2002;
542: 991-995
MissingFormLabel
- 41
Zhao J,
Lili L,
Cheung SS.
et al.
Hot environments decrease exercise capacity and elevate multiple
neurotransmitters. Life Sci 2015; 141: 74-80
MissingFormLabel
- 42
VanHaitsma TA,
Light AR,
Light KC,
Hughen RW,
Yenchik S,
White AT.
Fatigue sensation and gene expression in trained cyclists following a 40 km time
trial in the heat. Eur J Appl Physiol 2016; 116: 541-552
MissingFormLabel
- 43
Blegen M,
Cheatham C,
Caine-Bish N.
et al.
The immunological and metabolic responses to exercise of varying intensities in
normoxic and hypoxic environments. J Strength Cond Res 2008; 22: 1638-1644
MissingFormLabel
- 44
Khalafi M,
Sakhaei MH,
Symonds ME,
Noori Mofrad SR,
Liu Y,
Korivi M.
Impact of exercise in hypoxia on inflammatory cytokines in adults: a systematic
review and meta-analysis. Sports Med Open 2023; 9: 50
MissingFormLabel
- 45
Santos SA,
Lira FS,
Silva ET,
Caris AV,
Oyama LM,
Thomatieli-Santos RV.
Effect of moderate exercise under hypoxia on Th1/Th2 cytokine balance. Clin Respir
J 2019; 13: 583-589
MissingFormLabel
- 46
Hagobian TA,
Jacobs KA,
Subudhi AW.
et al.
Cytokine responses at high altitude: effects of exercise and antioxidants at
4300 m. Med Sci Sports Exerc 2006; 38: 276-285
MissingFormLabel
- 47
Hill GW,
Gillum TL,
Lee BJ,
Romano PA,
Schall ZJ,
Kuennen MR.
Reduced inflammatory and phagocytotic responses following normobaric hypoxia
exercise despite evidence supporting greater immune challenge. Appl Physiol Nutr Metab
2020; 45: 628-640
MissingFormLabel
- 48
Hall B,
Zebrowska A,
Kaminski T.
et al.
Effects of hypoxia during continuous and intermittent exercise on glycaemic
control and selected markers of vascular function in type 1 diabetes. Exp Clin Endocrinol
Diabetes 2018; 126: 229-241
MissingFormLabel
- 49
Thompson D,
Nicholas CW,
Williams C.
Muscular soreness following prolonged intermittent high-intensity shuttle
running. J Sports Sci 1999; 17: 387-395
MissingFormLabel
- 50
Minett GM,
Duffield R,
Kellett A,
Portus M.
Effects of mixed-method cooling on recovery of medium-fast bowling performance
in hot conditions on consecutive days. J Sports Sci 2012; 30: 1387-1396
MissingFormLabel
- 51
Álvarez-Herms J,
Julià-Sánchez S,
Gatterer H.
et al.
Anaerobic training in hypoxia: A new approach to stimulate the rating of effort
perception. Physiol Behav 2016; 163: 37-42
MissingFormLabel
- 52
Samuel MN,
Holcomb WR,
Guadagnoli MA.
et al.
Acute effects of static and ballistic stretching on measures of strength and
power. J Strength Cond Res 2008; 22: 1422-1428
MissingFormLabel
- 53
Scott BR,
Slattery KM,
Sculley DV.
et al.
Hypoxia during resistance exercise does not affect physical performance,
perceptual responses, or neuromuscular recovery. J Strength Cond Res 2018; 32: 2174-2182
MissingFormLabel
- 54
Carmo AAL,
Goulart KNO,
Cabido CET.
et al.
Active warm-up and time-of-day effects on repeated-sprint performance and
post-exercise recovery. Eur J Appl Physiol 2023; 123: 49-64
MissingFormLabel
- 55
Casadio JR,
Storey AG,
Merien F,
Kilding AE,
Cotter JD,
Laursen PB.
Acute effects of heated resistance exercise in female and male power
athletes. Eur J Appl Physiol 2017; 117: 1965-1976
MissingFormLabel
- 56
Pompeo A,
Afonso J,
Cirillo ELR.
et al.
Impact of temperature on physical and cognitive performance in elite female
football players during intermittent exercise. Scand J Med Sci Sports 2024; 34: e14646
MissingFormLabel
- 57
Girard O,
Mendez-Villanueva A,
Bishop D.
Repeated-sprint ability—part I: factors contributing to fatigue. Sports Med 2011;
41: 673-694
MissingFormLabel
- 58
Powers SK,
Nelson WB,
Hudson MB.
Exercise-induced oxidative stress in humans: cause and consequences. Free Radic Biol
Med 2011; 51: 942-950
MissingFormLabel
- 59
Slivka D,
Shute R,
Hailes W.
et al.
Exercise in the heat blunts improvements in aerobic power. Eur J Appl Physiol 2021;
121: 1715-1723
MissingFormLabel
- 60
Gandevia SC.
Spinal and supraspinal factors in human muscle fatigue. Physiol Rev 2001; 81: 1725-1789
MissingFormLabel
- 61
Debold EP.
Recent insights into the molecular basis of muscular fatigue. Med Sci Sports Exerc
2012; 44: 1440-1452
MissingFormLabel
- 62
Shimazaki Y,
Yoshida A,
Yamamoto T.
Thermal responses and perceptions under distinct ambient temperature and wind
conditions. J Therm Biol 2015; 49–50: 1-8
MissingFormLabel
- 63
Hargreaves M.
Physiological limits to exercise performance in the heat. J Sci Med Sport 2008; 11:
66-71
MissingFormLabel
- 64
Kaldur T,
Kals J,
Ööpik V.
et al.
Effects of heat acclimation on changes in oxidative stress and inflammation
caused by endurance capacity test in the heat. Oxid Med Cell Longev 2014; 2014: 107137
MissingFormLabel
- 65
Souza-Silva AA,
Moreira E,
de Melo-Marins D,
Schöler CM,
de Bittencourt PIH,
Laitano O.
High intensity interval training in the heat enhances exercise-induced lipid
peroxidation, but prevents protein oxidation in physically active men. Temperature
2016; 3: 167-175
MissingFormLabel
- 66
Périard JD,
Pyne DB,
Bishop DJ,
Wallett A,
Girard O.
Short-term repeated-sprint training in hot and cool conditions similarly
benefits performance in team-sport athletes. Front Physiol 2020; 11: 1023
MissingFormLabel
- 67
Meade RD,
Kenny GP.
Are all heat loads created equal?. Med Sci Sports Exerc 2017; 49: 1796-1804
MissingFormLabel
- 68
Pitsiladis YP,
Maughan RJ.
The effects of exercise and diet manipulation on the capacity to perform
prolonged exercise in the heat and in the cold in trained humans. J Physiol 1999;
517: 919-930
MissingFormLabel
- 69
Costello JT,
Rendell RA,
Furber M.
et al.
Effects of acute or chronic heat exposure, exercise and dehydration on plasma
cortisol, IL-6 and CRP levels in trained males. Cytokine 2018; 110: 277-283
MissingFormLabel
- 70
Sandiford SD,
Green HJ,
Duhamel TA,
Perco JG,
Schertzer JD,
Ouyang J.
Inactivation of human muscle Na+-K+-ATPase in vitro during prolonged exercise is
increased with hypoxia. J Appl Physiol 2004; 96: 1767-1775
MissingFormLabel