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Gastrointestinal Function, Damage and Symptoms During Exercise and the Potential Therapeutic Role of Probiotic Supplementation

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Gastrointestinal Function, Damage and Symptoms During Exercise and the Potential Therapeutic Role of Probiotic Supplementation Gastrointestinal Function, Damage and Symptoms During Exercise and the Potential Therapeutic Role of Probiotic Supplementation JAMIE NICHOLAS PUGH A thesis submitted in partial fulfilment of the requirements of Liverpool John Moores University for the degree of Doctor of Philosophy November 2018 Authors Declaration I declare that the work in this thesis was carried out in accordance with the regulations of Liverpool John Moores University. Apart from the help and advice acknowledged, the work within was solely completed and carried out by the author. Any views expressed in this thesis are those of the author and in no way represent those of Liverpool John Moores University and the School of Sport and Exercise Science. This thesis has not been presented to any other University for examination either in the United Kingdom or overseas. No portion of the work referred to in this research project has been submitted in support of an application for another degree or qualification of this or any other university or institute of learning. Copyright in text of this research project rests with the author. The ownership of any intellectual property rights, which may be described in this research project, is vested in Liverpool John Moores University and may not be made available for use to any third parties without the written permission of the University. Signed Date 2 Acknowledgements I would like to thank my director of studies Graeme Close. Thank you for taking a chance on me at the beginning. No one has afforded me as many opportunities over the last number of years and only your faith in me made it possible to devise and deliver on the final two studies of this thesis. I hope we continue some of the work we have started for many, many years to come. I would also like to thank Dominic Doran for giving me both the support and guidance to develop as a person and an academic over the course of the PhD. I will never be able to repay the hours spent in your office discussing ideas, results and problems throughout the last few years. Thank you. Thirdly, I would like to offer my thanks to James Morton. Your attention to detail and work ethic are an example to everyone in academia. The advice and feedback you give is second-to-none and so I appreciate the support you have given me. I wish to acknowledge Professor Anton Wagenmakers for his expertise and input into the design and analysis of data in Chapter 6, as well as Professor Barbara Fielding from the University of Surrey for the analysis of the samples. The lactulose:rhamnose analysis of all samples would not have been possible without the work of Dr Simon Fleming from the Royal Cornwall Hospital. None of the work in Chapter 7 would have been possible without Dr Andy Sparks from Edge Hill University. You truly went above and beyond to help me be able to run that study. From a chance introduction at an Ultramarathon around Edge Hill campus, who knew you would be helping me organise a track marathon at the same venue a year or so later. The data collection for the studies presented would never have been possible without the technical staff at LJMU – Gemma, Dean, and George, as well as countless PhD and MSc students who have helped me along the way. Finally, I owe a huge thank you to every single person that participated in one of the studies. The questions we ask would never be answered without you volunteering your time and efforts. 3 Dedication For my family. My mum and dad who, from even from early in life, have pushed me to be the best I can be. My brothers, Michael and Luke, and my sister Danielle. And finally to Sarah-Jayne for putting up with me, moving across the country for me (again), and for making me laugh every single day. 4 Publications and presented abstracts arising from this thesis: Publications Pugh, J. N., Impey, S. G., Doran, D. A., Fleming, S. C., Morton, J. P., & Close, G. L. (2017). Acute high- intensity interval running increases markers of gastrointestinal damage and permeability but not gastrointestinal symptoms. Applied Physiology, Nutrition, and Metabolism, 42(9), 941-947. Pugh, J., Kirk, B., Fearn, R., Morton, J., & Close, G. (2018). Prevalence, Severity and Potential Nutritional Causes of Gastrointestinal Symptoms during a Marathon in Recreational Runners. Nutrients, 10(7), 811. Abstract Pugh, J., Wagenmaker, A., Morton, J., Close, G. Probiotic supplementation increases CHO oxidation in trained male cyclists: a randomised, double-blind, placebo-controlled cross-over trial. Presented at European College of Sports Scientists, Dublin, Ireland 2018 Editorial Pugh, Jamie N., Robert Fearn, James P. Morton, and Graeme L. Close. "Gastrointestinal symptoms in elite athletes: time to recognise the problem?." (2017): bjsports-2017. 5 Abstract Gastrointestinal (GI) symptoms are widely reported in athletes participating in prolonged endurance events including; cyclists, triathletes and marathon runners, although there is a large estimated range of between 4–96% of participants affected (Costa et al., 2017a). Two potential causes of exercise- associated GI symptoms are exercise-induced increases in GI permeability and damage, and the consumption of carbohydrate (CHO) during exercise (Costa et al., 2017b, de Oliveira, 2017, de Oliveira and Burini, 2014). To date, the association between markers of GI damage or barrier disruption and GI symptoms during endurance exercise has been equivocal. Additionally, while CHO consumption enhances exercise capacity and performance (Stellingwerff and Cox, 2014), ingestion also appears to increase the risk of GI symptoms, although data is again equivocal (Costa et al., 2017a). Given this prevalence of GI symptoms, probiotics may offer a convenient and practical strategy to reduce exercise-associated GI symptoms, with evidence showing their capability to alter CHO absorption and metabolism along with attenuating exercise-induced GI permeability and damage. The aim of this thesis is to investigate the relationship between markers of GI permeability and damage, measured in the blood, and GI symptoms during endurance exercise, up to marathon distance running. The role of CHO intake in GI symptoms will be examined, as well as the use of probiotics to reduce such symptoms. To realise these aims, the following objectives will be addressed: 1) Investigate the prevalence and severity of exercise-associated GI symptoms (Chapters 4 and 7) 2) Explore the role of different circulatory markers to measure GI permeability and damage, and their relation to GI symptoms (Chapters 5, 6, and 7 ) 3) Investigate the use of probiotics in reducing GI symptoms exacerbated by CHO during prolonged exercise (Chapter 6 and 7) 4) Investigate the efficacy of probiotics to reduce GI permeability and damage during exercise (Chapter 6 and 7) The main findings from this thesis imply that a moderate prevalence of GI symptoms exists in recreational runners, with 27-58% of marathon participants having reported mild to severe GI symptoms during the race. Laboratory-based exercise protocols exhibited much lower symptom prevalence compared with marathon races. When markers of GI permeability and damage were assessed, there appeared to be no association between these and GI symptoms. One systemic measure that correlated to a number of GI symptoms during a marathon was CD14, a non-specific marker of monocyte activation. Probiotics had no measurable effect on markers of GI permeability and damage during a marathon race, however, probiotic supplementation had a small but significant effect on exercise metabolism during steady state cycling; with an increase in CHO oxidation and subsequent reduction in lipid oxidation. Probiotic supplementation was also associated with less severe GI symptoms during both a marathon race, and in the four weeks leading to it. Furthermore, 6 beneficial effects of probiotics on GI symptoms during the marathon were associated with better maintenance of running speed during the final third of the race. Taken together, GI symptoms are prevalent in endurance athletes. Symptom aetiology can vary but probiotics appear to be a promising strategy that can be used to not only reduce GI symptoms, but may even indirectly improve exercise performance. 7 Contents Gastrointestinal Function, Damage and Symptoms During Exercise and the Potential Therapeutic Role of Probiotic Supplementation ............................................................................................... 1 Acknowledgements...................................................................................................................... 3 Dedication ................................................................................................................................... 4 Publications and presented abstracts arising from this thesis: ....................................................... 5 Publications ........................................................................................................................................................ 5 Abstract .............................................................................................................................................................. 5 Editorial .............................................................................................................................................................. 5 Abstract ....................................................................................................................................... 6 Contents .....................................................................................................................................
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