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European Journal of Applied Physiology

, Volume 119, Issue 8, pp 1829–1840 | Cite as

The effect of cycling in the heat on gastrointestinal-induced damage and neuromuscular fatigue

  • John O. OsborneEmail author
  • Ian B. Stewart
  • Kenneth W. Beagley
  • Geoffrey M. Minett
Original Article

Abstract

Purpose

This study investigated the effect of exercise in the heat on neuromuscular function, gastrointestinal damage, endotoxemia and inflammatory cytokines.

Methods

Eight male cyclists completed two 60 min cycling trials in both hot (HOT 34.5 ± 0.1 °C and 53 ± 1% relative humidity) and temperate environments (CON 20.2 ± 0.3 °C and 55 ± 3% relative humidity). The cycling task comprised of alternating 3 min intervals at a moderate-vigorous intensity (50% and 70% of maximum power output; Pmax) for 30 min, followed by 30 min at moderate intensity (40–50% Pmax). Neuromuscular function was assessed at pre-, post-exercise and 60 min post-exercise. Circulating levels of endotoxins, inflammatory cytokines and markers of gut permeability and damage were also collected at these time points. Heart rate, core temperature, skin temperature, perceived exertion, thermal sensation and comfort were also measured.

Results

Post-exercise voluntary activation of HOT (87.9% [85.2, 90.8]) was statistically lower (mean difference − 2.5% [− 4.5, − 0.5], d = 2.50) than that of CON (90.5% [87.8, 93.2]). The HOT trial resulted in statistically elevated (+ 69%) markers of gastrointestinal damage compared to CON (mean difference 0.424 ng mL−1 [0.163, 0.684, d = − 3.26]), although this was not observed for endotoxin, other inflammatory markers, or gastrointestinal permeability.

Conclusions

This research provides evidence that short-duration cycling in the heat results in sub-optimal neuromuscular activation and increased expression of gastrointestinal damage markers, without a simultaneous elevation in circulating endotoxins or pro-inflammatory cytokines.

Keywords

Thermoregulation Endotoxemia Cycling Central fatigue Hyperthermia 

Abbreviations

½RT

Half relaxation time

CD

Contraction duration

CI

Credible interval

CLDN-3

Claudin 3

CNS

Central nervous system

CV

Coefficient of variation

ELISA

Enzyme-linked immunosorbent assay

EMG

Electromyography

HR

Heart rate

ICC

Intraclass correlation

I-FABP

Intestinal fatty acid-binding protein

IL-1β

Interleukin 1 beta

MCMC

Markov chain Monte Carlo

MD

Mean difference

MVC

Maximum voluntary contraction

Pmax

Maximal aerobic power output

Pt

Peak torque

RPE

Rating of perceived exertion

RR

Rate of relaxation

RTD

Rate of torque development

Tc

Core temperature

TNF-α

Tumour necrosis factor alpha

TPt

Time to peak torque

Tsk

Mean skin temperature

VA

Voluntary activation

VL

Vastus lateralis

VM

Vastus medialis

VO2max

Maximal aerobic capacity

Notes

Acknowledgements

The authors sincerely thank Mr Logan Trim (Institute of Health and Biomedical Innovation, Queensland University of Technology, Brisbane, Queensland, Australia) for his technical assistance with the immunoassay analysis.

Author contributions

Study conception and design: JOO, IBS, KWB and GMM. Data collection: JOO. Data analysis: JOO, IBS and GMM. Contributed materials/tools: GMM, KWB and IBS. Wrote manuscript: JOO. Drafted and approved manuscript: JOO, IBS, KWB and GMM.

Funding

None.

Compliance with ethical standards

Conflict of interests

The authors have no conflict of interests to declare.

References

  1. Allen GM, Gandevia SC, McKenzie DK (1995) Reliability of measurements of muscle strength and voluntary activation using twitch interpolation. Muscle Nerve 18:593–600.  https://doi.org/10.1002/mus.880180605 CrossRefPubMedGoogle Scholar
  2. Ament W, Verkerke GJ (2009) Exercise and fatigue. Sports Med 39:389–422.  https://doi.org/10.2165/00007256-200939050-00005 CrossRefPubMedGoogle Scholar
  3. Borg G (1970) Perceived exertion as an indicator of somatic stress. Scand J Rehabil Med 2:92–98Google Scholar
  4. Bosenberg AT, Brock-Utne JG, Gaffin SL, Wells MTB, Blake GTW (1988) Strenuous exercise causes systemic endotoxemia. J Appl Physiol 65:106–108CrossRefPubMedGoogle Scholar
  5. Burden A, Bartlett R (1999) Normalisation of EMG amplitude: an evaluation and comparison of old and new methods. Med Eng Phys 21:247–257.  https://doi.org/10.1016/S1350-4533(99)00054-5 CrossRefPubMedGoogle Scholar
  6. Byrne C, Lee JK, Chew SA, Lim CL, Tan EY (2006) Continuous thermoregulatory responses to mass-participation distance running in heat. Med Sci Sports Exerc 38:803–810.  https://doi.org/10.1249/01.mss.0000218134.74238.6a CrossRefPubMedGoogle Scholar
  7. Camus G, Poortmans J, Nys M, Deby-Dupont G, Duchateau J, Deby C, Lamy M (1997) Mild endotoxaemia and the inflammatory response induced by a marathon race. Clin Sci 92:415–422CrossRefPubMedGoogle Scholar
  8. Cannon J, Kay D, Tarpenning KM, Marino FE (2007) Comparative effects of resistance training on peak isometric torque, muscle hypertrophy, voluntary activation and surface EMG between young and elderly women. Clin Physiol Funct Imaging 27:91–100.  https://doi.org/10.1111/j.1475-097X.2007.00719.x CrossRefPubMedGoogle Scholar
  9. Cannon J, Kay D, Tarpenning KM, Marino FE (2008) Reproducibility and changes in twitch properties associated with age and resistance training in young and elderly women. Scand J Med Sci Sports 18:627–635.  https://doi.org/10.1111/j.1600-0838.2007.00709.x CrossRefPubMedGoogle Scholar
  10. Cheung SS (2007) Hyperthermia and voluntary exhaustion: integrating models and future challenges. Appl Physiol Nutr Metab 32:808–817.  https://doi.org/10.1139/H07-043 CrossRefPubMedGoogle Scholar
  11. Cheung SS, Sleivert GG (2004) Multiple triggers for hyperthermic fatigue and exhaustion. Exerc Sport Sci Rev 32:100–106.  https://doi.org/10.1097/00003677-200407000-00005 CrossRefPubMedGoogle Scholar
  12. Cohen J (1988) Statistical power analysis for the behavioral sciences, 2nd edn. L. Erlbaum Associates, HillsdaleGoogle Scholar
  13. Dantzer R (2004) Cytokine-induced sickness behaviour: a neuroimmune response to activation of innate immunity. Eur J Pharmacol 500:399–411.  https://doi.org/10.1016/j.ejphar.2004.07.040 CrossRefGoogle Scholar
  14. De Pauw K, Roelands B, Cheung SS, de Geus B, Rietjens G, Meeusen R (2013) Guidelines to classify subject groups in sport-science research. Int J Sports Physiol Perform 8:111–122CrossRefPubMedGoogle Scholar
  15. Ely BR, Ely MR, Cheuvront SN, Kenefick RW, Degroot DW, Montain SJ (2009) Evidence against a 40 °C core temperature threshold for fatigue in humans. J Appl Physiol 107:1519–1525.  https://doi.org/10.1152/japplphysiol.00577.2009 CrossRefPubMedGoogle Scholar
  16. Gagge AP, Stolwijk JA, Hardy JD (1967) Comfort and thermal sensations and associated physiological responses at various ambient temperatures. Environ Res 1:1–20CrossRefPubMedGoogle Scholar
  17. Gill SK et al (2015a) The impact of a 24-h ultra-marathon on circulatory endotoxin and cytokine profile. Int J Sports Med 36:688–695.  https://doi.org/10.1055/s-0034-1398535 CrossRefPubMedGoogle Scholar
  18. Gill SK et al (2015b) Circulatory endotoxin concentration and cytokine profile in response to exertional-heat stress during a multi-stage ultra-marathon competition. Exerc Immunol Rev 21:114–128PubMedGoogle Scholar
  19. Gnauck A, Lentle RG, Kruger MC (2016) Chasing a ghost? Issues with the determination of circulating levels of endotoxin in human blood. Crit Rev Clin Lab Sci 53:197–215.  https://doi.org/10.3109/10408363.2015.1123215 CrossRefPubMedGoogle Scholar
  20. Gray SR, Clifford M, Lancaster R, Leggate M, Davies M, Nimmo MA (2009) The response of circulating levels of the interleukin-6/interleukin-6 receptor complex to exercise in young men. Cytokine 47:98–102.  https://doi.org/10.1016/j.cyto.2009.05.011 CrossRefPubMedGoogle Scholar
  21. Grootjans J, Thuijls G, Verdam F, Derikx JP, Lenaerts K, Buurman WA (2010) Non-invasive assessment of barrier integrity and function of the human gut World. J Gastrointest Surg 2:61–69.  https://doi.org/10.4240/wjgs.v2.i3.61 CrossRefGoogle Scholar
  22. Habes QLM et al (2017) Markers of intestinal damage and their relation to cytokine levels in cardiac surgery patients. Shock 47:709–714CrossRefPubMedGoogle Scholar
  23. ISO 9886 (2004) Evaluation of thermal strain by physiological measurements. International Organization for Standardization, GenevaGoogle Scholar
  24. Jeukendrup AE, Vet-Joop K, Sturk A, Stegen JHJC, Senden J, Saris WHM, Wagenmakers AJM (2000) Relationship between gastro-intestinal complaints and endotoxaemia, cytokine release and the acute-phase reaction during and after a long-distance triathlon in highly trained men. Clin Sci 98:47–55.  https://doi.org/10.1042/CS19990258 CrossRefGoogle Scholar
  25. Lambert GP (2004) Role of gastrointestinal permeability in exertional heatstroke. Exerc Sport Sci Rev 32:185–190.  https://doi.org/10.1097/00003677-200410000-00011 CrossRefPubMedGoogle Scholar
  26. Lambert GP (2008) Intestinal barrier dysfunction, endotoxemia, and gastrointestinal symptoms: the 'canary in the coal mine' during exercise-heat stress? Med Sport Sci 53:61–73.  https://doi.org/10.1159/000151550 CrossRefGoogle Scholar
  27. Lambert GP (2009) Stress-induced gastrointestinal barrier dysfunction and its inflammatory effects. J Anim Sci 87:E101–E108.  https://doi.org/10.2527/jas.2008-1339 CrossRefGoogle Scholar
  28. Lim CL, Mackinnon LT (2006) The roles of exercise-induced immune system disturbances in the pathology of heat stroke: the dual pathway model of heat stroke. Sports Med 36:39–64CrossRefPubMedGoogle Scholar
  29. March DS, Marchbank T, Playford RJ, Jones AW, Thatcher R, Davison G (2017) Intestinal fatty acid-binding protein and gut permeability responses to exercise. Eur J Appl Physiol 117:931–941.  https://doi.org/10.1007/s00421-017-3582-4 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Marchbank T, Davison G, Oakes JR, Ghatei MA, Patterson M, Moyer MP, Playford RJ (2011) The nutriceutical bovine colostrum truncates the increase in gut permeability caused by heavy exercise in athletes. Am J Physiol Gastrointest Liver Physiol 300:G477–G484CrossRefGoogle Scholar
  31. Marshall JC (1998) The gut as a potential trigger of exercise-induced inflammatory responses. Can J Physiol Pharmacol 76:479–484.  https://doi.org/10.1139/y98-049 CrossRefPubMedGoogle Scholar
  32. Mengersen KL, Drovandi CC, Robert CP, Pyne DB, Gore CJ (2016) Bayesian estimation of small effects in exercise and sports science. PLoS ONE 11:e0147311.  https://doi.org/10.1371/journal.pone.0147311 CrossRefPubMedPubMedCentralGoogle Scholar
  33. Morris G, Berk M, Galecki P, Walder K, Maes M (2016) The neuro-immune pathophysiology of central and peripheral fatigue in systemic immune-inflammatory and neuro-immune diseases. Mol Neurobiol 53:1195–1219.  https://doi.org/10.1007/s12035-015-9090-9 CrossRefPubMedGoogle Scholar
  34. Moseley PL, Gapen C, Wallen ES, Walter ME, Peterson MW (1994) Thermal stress induces epithelial permeability. Am J Physiol Cell Physiol 267:C425–C434CrossRefGoogle Scholar
  35. Ng QY, Lee KW, Byrne C, Ho TF, Lim CL (2008) Plasma endotoxin and immune responses during a 21-km road race under a warm and humid environment. Ann Acad Med Singapore 37:307–314PubMedGoogle Scholar
  36. Nielsen B, Hales JR, Strange S, Christensen NJ, Warberg J, Saltin B (1993) Human circulatory and thermoregulatory adaptations with heat acclimation and exercise in a hot, dry environment. J Physiol 460:467–485CrossRefPubMedPubMedCentralGoogle Scholar
  37. Nybo L, González-Alonso J (2015) Critical core temperature: a hypothesis too simplistic to explain hyperthermia-induced fatigue. Scand J Med Sci Sports 25:4–5.  https://doi.org/10.1111/sms.12444 CrossRefPubMedGoogle Scholar
  38. Nybo L, Nielsen B (2001) Hyperthermia and central fatigue during prolonged exercise in humans. J Appl Physiol 91:1055–1060CrossRefPubMedGoogle Scholar
  39. Nybo L, Rasmussen P, Sawka MN (2014) Performance in the heat-physiological factors of importance for hyperthermia-induced fatigue. Compr Physiol 4:657–689.  https://doi.org/10.1002/cphy.c130012 CrossRefPubMedGoogle Scholar
  40. Pals KL, Chang R-T, Ryan AJ, Gisolfi CV (1997) Effect of running intensity on intestinal permeability. J Appl Physiol 82:571–576CrossRefPubMedGoogle Scholar
  41. Périard JD, Cramer MN, Chapman PG, Caillaud C, Thompson MW (2011) Neuromuscular function following prolonged intense self-paced exercise in hot climatic conditions. Eur J Appl Physiol 111:1561–1569.  https://doi.org/10.1007/s00421-010-1781-3 CrossRefPubMedGoogle Scholar
  42. Pugh JN, Impey SG, Doran DA, Fleming SC, Morton JP, Close GL (2017) Acute high-intensity interval running increases markers of gastrointestinal damage and permeability but not gastrointestinal symptoms. Appl Physiol Nutr Metab 42:941–947.  https://doi.org/10.1139/apnm-2016-0646 CrossRefGoogle Scholar
  43. Racinais S, Périard JD, Karlsen A, Nybo L (2015) Effect of heat and heat acclimatization on cycling time trial performance and pacing. Med Sci Sports Exerc 47:601–606.  https://doi.org/10.1249/MSS.0000000000000428 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Racinais S, Moussay S, Nichols D, Travers G, Belfekih T, Schumacher YO, Périard JD (2019) Core temperature up to 41.5 ºC during the UCI Road Cycling World Championships in the heat. Br J Sports Med 53:426–429.  https://doi.org/10.1136/bjsports-2018-099881 CrossRefPubMedGoogle Scholar
  45. Robson-Ansley PJ, Milander Ld, Collins M, Noakes TD (2004) Acute interleukin-6 administration impairs athletic performance in healthy trained male runners. Can J Appl Physiol 29:411–418.  https://doi.org/10.1139/h04-026 CrossRefPubMedGoogle Scholar
  46. Saboisky J, Marino FE, Kay D, Cannon J (2003) Exercise heat stress does not reduce central activation to non-exercised human skeletal muscle. Exp Physiol 88:783–790CrossRefPubMedGoogle Scholar
  47. Sharma HS, Hoopes PJ (2003) Hyperthermia induced pathophysiology of the central nervous system. Int J Hyperthermia 19:325–354.  https://doi.org/10.1080/0265673021000054621 CrossRefPubMedGoogle Scholar
  48. Shield A, Zhou S (2004) Assessing voluntary muscle activation with the twitch interpolation technique. Sports Med 34:253–267.  https://doi.org/10.2165/00007256-200434040-00005 CrossRefPubMedGoogle Scholar
  49. Shing CM et al (2014) Effects of probiotics supplementation on gastrointestinal permeability, inflammation and exercise performance in the heat. Eur J Appl Physiol 114:93–103.  https://doi.org/10.1007/s00421-013-2748-y CrossRefPubMedGoogle Scholar
  50. Tatterson AJ, Hahn AG, Martini DT, Febbraio MA (2000) Effects of heat stress on physiological responses and exercise performance in elite cyclists. J Sci Med Sport 3:186–193.  https://doi.org/10.1016/S1440-2440(00)80080-8 CrossRefPubMedGoogle Scholar
  51. Thuijls G et al (2010) Urine-based detection of intestinal tight junction loss. J Clin Gastroenterol 44:e14–19.  https://doi.org/10.1097/MCG.0b013e31819f5652 CrossRefPubMedGoogle Scholar
  52. Todd G, Butler JE, Taylor JL, Gandevia SC (2005) Hyperthermia: a failure of the motor cortex and the muscle. J Physiol 563:621–631.  https://doi.org/10.1113/jphysiol.2004.077115 CrossRefPubMedGoogle Scholar
  53. Tucker R, Rauch L, Harley YXR, Noakes TD (2004) Impaired exercise performance in the heat is associated with an anticipatory reduction in skeletal muscle recruitment. Pflugers Arch Eur J Physiol 448:422–430.  https://doi.org/10.1007/s00424-004-1267-4 CrossRefGoogle Scholar
  54. van Nieuwenhoven MA, Brouns F, Brummer R-JM (2004) Gastrointestinal profile of symptomatic athletes at rest and during physical exercise. Eur J Appl Physiol 91:429–434.  https://doi.org/10.1007/s00421-003-1007-z CrossRefPubMedGoogle Scholar
  55. van Wijck K, Lenaerts K, van Loon LJ, Peters WH, Buurman WA, Dejong CH (2011) Exercise-induced splanchnic hypoperfusion results in gut dysfunction in healthy men. PLoS ONE 6:e22366.  https://doi.org/10.1371/journal.pone.0022366 CrossRefPubMedPubMedCentralGoogle Scholar
  56. Vargas NT, Marino F (2014) A neuroinflammatory model for acute fatigue during exercise. Sports Med 44:1479–1487.  https://doi.org/10.1007/s40279-014-0232-4 CrossRefPubMedGoogle Scholar
  57. Vargas N, Marino F (2017) Neuroinflammation, cortical activity, and fatiguing behaviour during self-paced exercise. Pflugers Arch Eur J Physiol 470:413–426.  https://doi.org/10.1007/s00424-017-2086-8 CrossRefGoogle Scholar
  58. Vezzani A, Viviani B (2015) Neuromodulatory properties of inflammatory cytokines and their impact on neuronal excitability. Neuropharmacology 96:70–82.  https://doi.org/10.1016/j.neuropharm.2014.10.027 CrossRefPubMedGoogle Scholar
  59. Vitkovic L, Bockaert J, Jacque C (2000) “Inflammatory” cytokines: neuromodulators in normal brain? J Neurochem 74:457–471.  https://doi.org/10.1046/j.1471-4159.2000.740457.x CrossRefPubMedGoogle Scholar
  60. Yeh YJ, Law LYL, Lim CL (2013) Gastrointestinal response and endotoxemia during intense exercise in hot and cool environments. Eur J Appl Physiol 113:1575–1583.  https://doi.org/10.1007/s00421-013-2587-x CrossRefPubMedGoogle Scholar
  61. Young AJ, Sawka MN, Epstein Y, Decristofano B, Pandolf KB (1987) Cooling different body surfaces during upper and lower body exercise. J Appl Physiol 63:1218–1223CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.School of Exercise and Nutrition SciencesQueensland University of TechnologyBrisbaneAustralia
  2. 2.Institute of Health and Biomedical InnovationQueensland University of TechnologyBrisbaneAustralia
  3. 3.School of Biomedical SciencesQueensland University of TechnologyBrisbaneAustralia

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