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John Owen Osborne Thesis GASTROINTESTINAL DAMAGE, INFLAMMATION AND CENTRAL FATIGUE DURING EXERCISE IN THE HEAT John Owen Osborne Bachelor of Exercise and Nutrition Sciences (Hons) Submitted in fulfilment of the requirements for the degree of Doctor of Philosophy School of Exercise and Nutrition Sciences Faculty of Health Queensland University of Technology 2019 Keywords endotoxemia exercise heat stress thermoregulation central fatigue cycling cytokines gastrointestinal permeability glutamine supplementation heat acclimation hyperthermia LPS neuromuscular performance inflammation ii Gastrointestinal damage, inflammation and central fatigue during exercise in the heat Abstract Exercise in the heat results in reduced performance due to an earlier onset of fatigue. This issue is relevant to both professional and recreational athletes, as well as certain military and civilian occupations. Current literature suggests that some of this impairment in exercise performance may potentially arise from a centrally-mediated decrease in muscle activation. However, the causal link between exercise, heat and central fatigue remains equivocal. During exercise in the heat, high core temperatures and reductions in gut blood flow increase the permeability of the gastrointestinal lining to endotoxins, which translocate through the damaged barrier and into systemic circulation. An elevation in circulating endotoxins triggers the release of pro-inflammatory cytokines, which have been linked to the occurrence of fatigue, and may modulate neuronal activity. This PhD investigated the relationship between exercise performance in the heat, gut damage, endotoxin release, inflammatory cytokines, and neuromuscular function. The initial proof-of-concept study found that 60 min of moderate-to-vigorous cycling in the heat resulted in a significant decrease in voluntary activation of knee extensor muscles and an elevation in circulating markers of gut damage, compared to a temperate condition. However, no condition differences were observed for endotoxin concentration, level of inflammatory cytokines or intestinal permeability. The findings from this study suggest that exercise in the heat results in diminished neuromuscular activation and hyperthermia-induced gut damage. The second study investigated the efficacy of glutamine supplementation on the performance of twelve well-trained cyclists during a 20 km time trial in the heat. Although glutamine did not improve cycling performance over a placebo, it was Gastrointestinal damage, inflammation and central fatigue during exercise in the heat iii observed to maintain voluntary strength and attenuate an increase in particular inflammatory cytokines and markers of gut damage. The findings from this study provided evidence that glutamine supplementation does not benefit shorter duration (~33 min) cycling tasks in the heat. However, glutamine-mediated protection of gut barrier integrity and reduced inflammation, resulting in improved preservation of knee extensor strength, could potentially enhance athletic performance over longer-duration exercise protocols, common in many competitive events (e.g., marathons, triathlons, time trials). Finally, the third investigation examined the effect of 5 days of heat acclimation training on 20 km time trial cycling performance in the heat, inflammation and neuromuscular performance. Heat acclimation was found to improve both 20 km performance and knee extensor strength, without inducing additional inflammatory stress, central fatigue or gut damage. In contrast, 5 days of training in thermoneutral conditions did not enhance self-paced 20 km performance in the heat and voluntary strength was reduced from initial baseline values, possibly due to cumulative peripheral fatigue. In conclusion, the data from this study supported an ergogenic effect from short-term heat acclimation training for athletes who undertook strenuous exercise in the heat. Moreover, the similar level of central fatigue and inflammation following heat acclimation, despite a larger workload, indicated that this intervention might preserve neuromuscular function and protect against exertional-endotoxemia. Collectively, this body of work demonstrates that strenuous exercise in the heat damages the gastrointestinal tract, impairs voluntary activation of skeletal muscle, and may result in elevated pro-inflammatory cytokines. In contrast to the thesis hypothesis and previous literature, hyperthermic exercise did not induce detectable endotoxin translocation, despite inflammation and central fatigue. This outcome potentially iv Gastrointestinal damage, inflammation and central fatigue during exercise in the heat suggests that transient endotoxemia is unlikely to be a mechanistic link between elevated core temperatures and CNS-mediated downregulation of voluntary drive during exercise in the heat. However, the findings of this PhD do tentatively support a possible association between heat, gut damage, inflammation and diminished neuromuscular function. Acute (i.e., glutamine) or chronic (i.e., heat acclimation) interventions that disrupt this cascade may result in beneficial performance improvements. Gastrointestinal damage, inflammation and central fatigue during exercise in the heat v Table of Contents Keywords ............................................................................................................................ ii Abstract .............................................................................................................................. iii Table of Contents ................................................................................................................ vi List of Figures .................................................................................................................. viii List of Tables ....................................................................................................................... x List of Abbreviations ......................................................................................................... xii Statement of Original Authorship ...................................................................................... xiv Publications......................................................................................................... xvii Chapter 1: Introduction ................................................................................... 1 1.1 Summary ................................................................................................................... 5 Chapter 2: Literature Review .......................................................................... 8 2.1 Thermoregulation during exercise .............................................................................. 8 2.2 Exercise performance in the heat ................................................................................ 9 2.3 Models of fatigue in the heat .................................................................................... 11 2.3.1 Critical core temperature theory ..................................................................... 12 2.3.2 Cardiovascular factors .................................................................................... 14 2.3.3 Central nervous system factors ....................................................................... 16 2.4 Neuroinflammatory fatigue ...................................................................................... 19 2.4.1 Exertional endotoxemia .................................................................................. 20 2.5 Protective Interventions............................................................................................ 32 2.5.1 Glutamine Supplementation ........................................................................... 33 2.5.2 Heat Acclimation ........................................................................................... 41 2.6 Summary and Implications ....................................................................................... 53 Chapter 3: Study 1 – The effects of cycling in the heat on gastrointestinal inflammation and neuromuscular fatigue. .......................................................... 54 3.1 Abstract ................................................................................................................... 54 3.2 Introduction ............................................................................................................. 55 3.3 Methods ................................................................................................................... 57 3.4 Results ..................................................................................................................... 66 3.5 Discussion ............................................................................................................... 72 3.6 Conclusion ............................................................................................................... 77 3.7 Acknowledgments ................................................................................................... 78 3.8 Linking Section ........................................................................................................ 84 Chapter 4: Study 2 – Glutamine supplementation does not improve 20 km cycling time trial performance in the heat. .......................................................... 87 4.1 Abstract ..................................................................................................................
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