The influence of a hot environment on physiological stress responses in exercise until exhaustion

RESEARCH ARTICLE The influence of a hot environment on physiological stress responses in exercise until exhaustion Romeu P. M. Silva1,2, Cristiano L. M. Barros2,3, Thiago T. Mendes2,3, Emerson S. Garcia2,3, Vitor E. Valenti ID4, Luiz Carlos de Abreu2, David M. Garner ID2,5, Foued Salmen Espindola1,2, Nilson Penha-Silva1,2* a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 OPEN ACCESS Citation: Silva RPM, Barros CLM, Mendes TT, Garcia ES, Valenti VE, de Abreu LC, et al. (2019) The influence of a hot environment on physiological stress responses in exercise until exhaustion. PLoS ONE 14(2): e0209510. https:// doi.org/10.1371/journal.pone.0209510 Editor: Caroline Sunderland, Nottingham Trent University, UNITED KINGDOM Received: September 11, 2018 Accepted: December 6, 2018 Published: February 6, 2019 Copyright: © 2019 Silva et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 1 Institute of Biotechnology, Federal University of Uberlandia, Uberlandia, MG, Brazil, 2 Department of Physiology and Morphology, School of Medicine of ABC, Santo Andre, SP, Brazil, 3 Federal University of Acre, Rio Branco, AC, Brazil, 4 Post-Graduate Program in Physical Therapy, UNESP, Presidente Prudente, SP, Brazil, 5 Cardiorespiratory Research Group, Department of Biological and Medical Sciences, Faculty of Health and Life Sciences, Oxford Brookes University, Headington Campus, Oxford, United Kingdom * , Abstract Exhaustive exercise in a hot environment can impair performance. Higher epinephrine plasma levels occur during exercise in heat, indicating greater sympathetic activity. This study examined the influence of exercise in the heat on stress levels. Nine young healthy men performed a maximal progressive test on a cycle ergometer at two different environmental conditions: hot (40˚C) and normal (22˚C), both between 40% and 50% relative humidity. Venous blood and saliva samples were collected pre-test and post-test. Before exercise there were no significant changes in salivary biomarkers (salivary IgA: p = 0.12; αamylase: p = 0.66; cortisol: p = 0.95; nitric oxide: p = 0.13; total proteins: p = 0.07) or blood lactate (p = 0.14) between the two thermal environments. Following exercise, there were significant increases in all variables (salivary IgA 22˚C: p = 0.04, 40˚C: p = 0.0002; α-amylase 22˚C: p = 0.0002, 40˚C: p = 0.0002; cortisol 22˚C: p = 0.02, 40˚C: p = 0.0002; nitric oxide 22˚C: p = 0.0005, 40˚C: p = 0.0003, total proteins 22˚C: p<0.0001, 40˚C: p<0.0001 and; blood lactate 22˚C: p<0.0001, 40˚C: p<0.0001) both at 22˚C and 40˚C. There was no significant adjustment regarding IgA levels between the two thermal environments (p = 0.74), however the levels of α-amylase (p = 0.02), cortisol (p<0.0001), nitric oxide (p = 0.02) and total proteins (p = 0.01) in saliva were higher in the hotter conditions. Blood lactate was lower under the hot environment (p = 0.01). In conclusion, enduring hot temperature intensified stressful responses elicited by exercise. This study advocates that hot temperature deteriorates exercise performance under exhaustive stress and effort conditions. Data Availability Statement: All relevant date are in the paper and its Supporting Information files. Funding: The authors did not receive specific financial funding. The equipments used were supported by CNPq and Capes (National Brazilian Foundation of support to research). Introduction Competing interests: The authors have declared that no competing interests exist. Physical activity induces physiological adjustment to support bodily changes during exercise. This adjustment varies with the duration [1], types and intensity of exercise [2], training level PLOS ONE | https://doi.org/10.1371/journal.pone.0209510 February 6, 2019 1 / 14 Hot temperature and exhaustive exercise [3] and environmental conditions [4]. The analysis of salivary components such as total protein, α-amylase, immunoglobulin A (IgA), nitric oxide (NO) and cortisol may signify a noninvasive technique to determine the relationship of the intensity, duration, temperature, relative humidity and type of exercise with the changes that these situations could cause on the immune system and on the physical stress of the athlete [4–6]. Several studies have investigated the effects of exercise in different situations on the immunological system by salivary IgA and have reported decreased [7], increased [8] or unchanged [9] IgA levels post exercise. A scientific investigation demonstrated that a 100-km ultra-marathon induced negative immunological changes [10]. As a consequence, the authors recommended that exhaustive physical exercise would cause increased vulnerability to infections [10]. In this way, the stress response induced by exercise can be evaluated through the activity of salivary α-amylase [6, 11, 12], which is regulated by the adrenal sympathetic system, by means of the action of norepinephrine on the salivary glands. The physical and psychological strain generated by exercise stimulates the release of a glucocorticoid hormone cortisol by the adrenal gland [13,14], promoting mood deviations and decreased athletic performance [1,14]. This is because the increase in cortisol is bound to decreased action of serotonin in the brain, by lessening of mRNA coding for the synthesis of this neurotransmitter receptor [15]. The abovementioned studies support the analysis of levels of α-amylase and cortisol in saliva as reliable parameters to estimate the stress induced by exercise [1,6]. The stress response is connected with exercise intensity, which can be analyzed through lactate. Blood lactate levels are useful to determine the critical intensity of physical exercise tolerance or alternatively to assess the level of athletic training [16]. The increase in salivary levels of total protein during exercise is attributable to activation of the sympathetic nervous system [17,18] and thus expresses the level of exercise-induced stress. Prolonged exercise commenced in a hot environment can impair the subject’s performance [19], as higher plasma concentrations of epinephrine during exercise elicited by heat induces higher sympathetic activity [20]. It has already been demonstrated that moderate-intensity exercise in a hot environment induced inflammatory processes [21] and that blood lactate responses to submaximal and maximal exercises are decreased under cool (10˚C) or hot (35˚C) conditions in soccer players [22]. Accordingly, it was recommended that athletes train in the morning during hot conditions, indicating the impact of hot temperature on immunological variables [23]. Declined salivary IgA accompanied by increased salivary α-amylase was reported in athletic runners during completion of an ultramarathon performed in hot conditions [24]. Recently, a (...truncated)