A novel strategy to reduce exercise-induced hyperthermia in different age groups

Supervised by:
  1. Roberto Aguado Jiménez Director

Defence university: Universidad Pública de Navarra

Fecha de defensa: 06 October 2016

  1. Juan del Coso Garrigós Chair
  2. Miguel Angel Barajas Vélez Secretary
  3. Cristina Granados Domínguez Committee member

Type: Thesis


Exercise and heat stress The limitations to exercise performances have been a matter of interest that have fascinated humans throughout history. There are a number of factors that may influence the capacity of an individual to perform prolonged exercise, one of which is ambient temperature.1 In 1916, Lee and Scott 2 were the first scientists who observed an early fatigue in cats during exercise in a hot environment. Although their results were inconclusive, they were the first authors to report that exercising in the heat leads to a premature fatigue. Following research done in humans, demonstrated that endurance could be impaired in hot environments when compared to temperate climates.1, 3, 4 As an example, Parkin at al.4 investigated the effects of three different ambient temperatures (3, 20 and 40ºC) on exercise performance during fatiguing submaximal exercise (70% peak pulmonary oxygen uptake). Authors observed a progressive decline in exercise as ambient temperature increases. However, the reasons for a diminished exercise performance in hot environment compared to the rest of ambient temperatures is still debated and it is considered to be multifactorial, as it will depend on the type of exercise, training status, motivation of the participants, acclimatization and/or hydration status.8 During the last century there has been a great effort from the scientific community in order to understand the complexity of hyperthermia-induced fatigue. It is considered that different physiological factors might limit maximal intensity exercise than submaximal intensity aerobic performance when exercising in the heat.5 For maximal intensity exercise, cardiovascular mechanisms related to oxygen delivery are likely to limit aerobic performance in the heat.6 High skin temperatures and the resulting elevation in skin blood flow are associated with impaired cardiac filling, reductions in end-diastolic volume and heart rate increases as an attempt to compensate a decreased stroke volume.5 Whereas for submaximal exercise, it seems to be more complex and interaction between several physiological factors may be responsible for inducing premature fatigue during prolonged exercise in the heat.7, 8 One of these physiological factors, a critically high level of body temperature ~40ºC, was proposed by Nielsen et al.3 to be the main factor limiting endurance performance in hot environments. Thirteen trained participants, exercised at 60% peak oxygen uptake at an ambient temperature of 40ºC and 10% relative humidity for 9-12 consecutive days and observed that fatigue occurred when participants reached a core temperature of 39.7ºC despite large improvements in exercise performance (from 48 to 80 minutes). Six years later, Gonzalez-Alonso and colleagues,9 observed similar results in seven trained cyclists who exercised at 60% maximal oxygen uptake in the heat (40ºC) until volitional exhaustion. Again, all participants fatigued at an identical level of hyperthermia (esophageal temperatures of 40.1-40.2ºC), regardless different initial temperatures. Authors from both studies concluded that a high body temperature, per se, was the main factor for exhaustion during exercise in heat stress. These studies formed the basis of the belief that high core temperature might be important for impairing exercise performance. Temperature regulation mechanisms Maintaining thermal balance in a hot environment is not only critical to preserving life and reducing heat illnesses; it is also essential in order to prevent decrements in athletic performance.11 It is well known that more than 75% of the energy that is generated by skeletal muscle substrate oxidation is released as heat.10 In order to promote heat loss, excess heat is transported from the core to the skin and then to the environment. Once the metabolic heat is transferred to the skin, there are various ways in which it can be lost to the environment, including radiation, conduction, convection and evaporation.10 During rest in a thermoneutral environment, radiation accounts for approximate 60% of total heat loss, conduction and convection for 15% and evaporation for 25%. These percentages will change during exercise, where evaporation will be the main mechanism of heat loss. According to the heat balance equation, when heat gain exceeds heat loss, body heat storage increases, elevating body temperature. During fixed-intensity (constant power) exercise, metabolic heat production is constant, and therefore, heat loss is limited only to autonomic responses.12 Consequently, core body temperature rises until heat balance is achieved as indicated by a ‘plateau’ in core temperature.13, 14 However, during fixed-intensity exercise in a hot environment, the heat balance is impossible to achieve; therefore, core temperature will rise linearly until exhaustion occurs. The inability to continue exercising in a hot environment is directly associated with the failure to achieve heat balance as heat exhaustion is accompanied by high core temperatures and an increased challenge for the cardiovascular system to simultaneously meet the demands for both the working musculature and temperature regulation.12 Aging: A risk factor for heat stress The ability to physiologically maintain body core temperature during heat stress becomes compromised with age.15 Individuals over the age of 60 years are the most vulnerable population during heat waves.16 Adults in this age group experience greater thermal strain during passive heat exposures 17, 18 and this could be heightened when exercising in the heat.19 Furthermore, age-related reductions in whole-body heat loss capacity are evident when exercising in hot environments.20, 21 This progressive reduction in the thermoregulatory ability can be associated with reduced sweat gland outputs, decreased skin blood flow, smaller increase in cardiac output and/or less redistribution of blood flow from renal and splanchnic circulations.22 Moreover, the problem can be exacerbated by the decreases in overall physical fitness and increases in body adiposity that may accompany aging, and experts have suggested that, in combination, these age-related changes in thermoregulatory and cardiovascular function can decrease the body’s ability to maintain body core temperature at safe levels, especially during extended exposure to heat or to physical activity in the heat.19 However, older adults up to the seventh decade of life and who are well trained, can safely complete the same relative workloads, comparing to moderately trained young men, without an increased risk of heat stress or heat stroke.23 Conversely, older adults show a decreased ability to sense and adapt to dehydration. In physiology studies in which dehydration was induced through heat exposure alone, through physical activity in the heat or through hypertonic saline infusion, healthy older individuals displayed lower subjective levels of thirst, decreased plasma volume and reduced water intake while dehydrated relative to younger counterparts.19 Furthermore, recovery from dehydration is prolonged in older adults, which may exacerbate their risk of heat-related injuries during extended periods of heat exposure. Strategies to reduce hyperthermia Over the last decade, there has been an increasing interest in designing intervention strategies to reduce and/or delay increases in core temperature and therefore enhance exercise performance. This topic is, this year again, becoming relevant with such an important sport event as it is Rio 2016 Olympics, where it is expected to reach temperatures of up to 30ºC and 60% relative humidity. According to the review by Wendt and colleagues,10 there are two main strategies that have been proven to be particularly effective in reducing health problems and performance decrements associated with hot environments: heat acclimatization and rehydration. In recent years, many other different strategies have been put in practice in order to prevent and/or delay increases in core temperature. Examples include ice-water immersion, ice-pack application, continual dousing with water combined with fanning,24 ice slurry ingestion 25 or the use of compression garments 26 to name a few. Compression garments. Studies on compression garments have recently emerged although fundamental effects on thermoregulatory strain remain equivocal.27 Claims from manufacturers include enhanced comfort perception,28 increased muscle blood flow and/or enhanced lactate removal.29 Further, recent developments in these garments have led to claims of thermoregulatory benefits attributed to increased heat dissipation as a result of improved sweat efficiency. However, this remains a contentious issue, as there remains a lack of research supporting these statements. While the use of lower body compression garments seems to be widely studied,26, 28, 30-32 there is limited research regarding the effects of wearing upper body compression garments. It has been shown that when male athletes exercise at 55% and 75% of the maximal oxygen consumption in moderate warm conditions (25ºC and 50% relative humidity), the highest sweat rates occur on the central (upper and mid) and lower back.33 As the evaporation of the sweat from the skin surface is the main mechanism to reduce heat storage during exercise, clothing designs that facilitate the heat dissipation in the upper body through compression may lead to lower body temperature increments and therefore delay the appearance of hyperthermia during exercise. References 1. Galloway SD, Maughan RJ. Effects of ambient temperature on the capacity to perform prolonged cycle exercise in man. Med Sci Sports Exerc. 1997 Sep;29(9):1240-9. PubMed PMID: 9309637. 2. Lee FS, Scott EL. The action of temperature and humidity on the working power of muscles and on the sugar of the blood. American Journal of Physiology -- Legacy Content. 1916 1916-05-01 00:00:00;40(3):486-501. 3. Nielsen B, Hales JR, Strange S, Christensen NJ, Warberg J, Saltin B. Human circulatory and thermoregulatory adaptations with heat acclimation and exercise in a hot, dry environment. J Physiol. 1993 Jan;460:467-85. PubMed PMID: 8487204. Pubmed Central PMCID: PMC1175224. 4. Parkin JM, Carey MF, Zhao S, Febbraio MA. Effect of ambient temperature on human skeletal muscle metabolism during fatiguing submaximal exercise. J Appl Physiol (1985). 1999 Mar;86(3):902-8. PubMed PMID: 10066703. 5. Nybo L, Rasmussen P, Sawka MN. Performance in the heat-physiological factors of importance for hyperthermia-induced fatigue. Compr Physiol. 2014 Apr;4(2):657-89. PubMed PMID: 24715563. 6. Gonzalez-Alonso J, Calbet JA. Reductions in systemic and skeletal muscle blood flow and oxygen delivery limit maximal aerobic capacity in humans. Circulation. 2003 Feb 18;107(6):824-30. PubMed PMID: 12591751. 7. Nybo L. Cycling in the heat: performance perspectives and cerebral challenges. Scand J Med Sci Sports. 2010 Oct;20 Suppl 3:71-9. PubMed PMID: 21029193. 8. Nybo L. Brain temperature and exercise performance. Exp Physiol. 2012 Mar;97(3):333-9. PubMed PMID: 22125311. 9. Gonzalez-Alonso J, Teller C, Andersen SL, Jensen FB, Hyldig T, Nielsen B. Influence of body temperature on the development of fatigue during prolonged exercise in the heat. J Appl Physiol (1985). 1999 Mar;86(3):1032-9. PubMed PMID: 10066720. 10. Wendt D, van Loon LJ, Lichtenbelt WD. Thermoregulation during exercise in the heat: strategies for maintaining health and performance. Sports Med. 2007;37(8):669-82. PubMed PMID: 17645370. 11. Davis JK, Bishop PA. Impact of clothing on exercise in the heat. Sports Med. 2013 Aug;43(8):695-706. PubMed PMID: 23620245. 12. Schlader ZJ, Raman A, Morton RH, Stannard SR, Mundel T. Exercise modality modulates body temperature regulation during exercise in uncompensable heat stress. Eur J Appl Physiol. 2011 May;111(5):757-66. PubMed PMID: 20978782. 13. Nielsen B, Nielsen M. Body temperature during work at different environmental temperatures. Acta Physiol Scand. 1962 Oct;56:120-9. PubMed PMID: 13938500. 14. Saltin B, Hermansen L. Esophageal, rectal, and muscle temperature during exercise. J Appl Physiol. 1966 Nov;21(6):1757-62. PubMed PMID: 5929300. 15. Inbar O, Morris N, Epstein Y, Gass G. Comparison of thermoregulatory responses to exercise in dry heat among prepubertal boys, young adults and older males. Exp Physiol. 2004 Nov;89(6):691-700. PubMed PMID: 15328309. 16. Rey G, Jougla E, Fouillet A, Pavillon G, Bessemoulin P, Frayssinet P, et al. The impact of major heat waves on all-cause and cause-specific mortality in France from 1971 to 2003. Int Arch Occup Environ Health. 2007 Jul;80(7):615-26. PubMed PMID: 17468879. Pubmed Central PMCID: PMC2291483. 17. Dufour A, Candas V. Ageing and thermal responses during passive heat exposure: sweating and sensory aspects. Eur J Appl Physiol. 2007 May;100(1):19-26. PubMed PMID: 17242944. 18. Armstrong CG, Kenney WL. Effects of age and acclimation on responses to passive heat exposure. J Appl Physiol (1985). 1993 Nov;75(5):2162-7. PubMed PMID: 8307874. 19. Kenny GP, Yardley J, Brown C, Sigal RJ, Jay O. Heat stress in older individuals and patients with common chronic diseases. CMAJ. 2010 Jul 13;182(10):1053-60. PubMed PMID: 19703915. Pubmed Central PMCID: PMC2900329. 20. Stapleton JM, Poirier MP, Flouris AD, Boulay P, Sigal RJ, Malcolm J, et al. Aging impairs heat loss, but when does it matter? J Appl Physiol (1985). 2015 Feb 1;118(3):299-309. PubMed PMID: 25505030. Pubmed Central PMCID: PMC4312844. 21. Larose J, Boulay P, Sigal RJ, Wright HE, Kenny GP. Age-related decrements in heat dissipation during physical activity occur as early as the age of 40. PLoS One. 2013;8(12):e83148. PubMed PMID: 24349447. Pubmed Central PMCID: PMC3861480. 22. Kenney WL, Munce TA. Invited review: aging and human temperature regulation. J Appl Physiol (1985). 2003 Dec;95(6):2598-603. PubMed PMID: 14600165. 23. Best S, Caillaud C, Thompson M. The effect of ageing and fitness on thermoregulatory response to high-intensity exercise. Scand J Med Sci Sports. 2012 Aug;22(4):e29-37. PubMed PMID: 22092378. 24. McDermott BP, Casa DJ, Ganio MS, Lopez RM, Yeargin SW, Armstrong LE, et al. Acute whole-body cooling for exercise-induced hyperthermia: a systematic review. J Athl Train. 2009 Jan-Feb;44(1):84-93. PubMed PMID: 19180223. Pubmed Central PMCID: PMC2629045. 25. Ross ML, Garvican LA, Jeacocke NA, Laursen PB, Abbiss CR, Martin DT, et al. Novel precooling strategy enhances time trial cycling in the heat. Med Sci Sports Exerc. 2011 Jan;43(1):123-33. PubMed PMID: 20508537. 26. Goh SS, Laursen PB, Dascombe B, Nosaka K. Effect of lower body compression garments on submaximal and maximal running performance in cold (10 degrees C) and hot (32 degrees C) environments. Eur J Appl Physiol. 2011 May;111(5):819-26. PubMed PMID: 21046140. 27. MacRae BA, Laing RM, Niven BE, Cotter JD. Pressure and coverage effects of sporting compression garments on cardiovascular function, thermoregulatory function, and exercise performance. Eur J Appl Physiol. 2012 May;112(5):1783-95. PubMed PMID: 21901265. 28. Ali A, Creasy RH, Edge JA. Physiological effects of wearing graduated compression stockings during running. Eur J Appl Physiol. 2010 Aug;109(6):1017-25. PubMed PMID: 20354717. 29. Houghton LA, Dawson B, Maloney SK. Effects of wearing compression garments on thermoregulation during simulated team sport activity in temperate environmental conditions. J Sci Med Sport. 2009 Mar;12(2):303-9. PubMed PMID: 18078787. 30. Ali A, Caine MP, Snow BG. Graduated compression stockings: physiological and perceptual responses during and after exercise. J Sports Sci. 2007 Feb 15;25(4):413-9. PubMed PMID: 17365528. 31. Barwood MJ, Corbett J, Feeney J, Hannaford P, Henderson D, Jones I, et al. Compression garments: no enhancement of high-intensity exercise in hot radiant conditions. Int J Sports Physiol Perform. 2013 Sep;8(5):527-35. PubMed PMID: 23349313. 32. Chatard JC, Atlaoui D, Farjanel J, Louisy F, Rastel D, Guezennec CY. Elastic stockings, performance and leg pain recovery in 63-year-old sportsmen. Eur J Appl Physiol. 2004 Dec;93(3):347-52. PubMed PMID: 15455235. 33. Smith CJ, Havenith G. Body mapping of sweating patterns in male athletes in mild exercise-induced hyperthermia. Eur J Appl Physiol. 2011 Jul;111(7):1391-404. PubMed PMID: 21153660.