Dietary carbohydrate, exercise, and human health

Abstract

For clarity, this thesis is separated into two parts: Part 1: Digestible carbohydrate and gastroenteropancreatic hormone release during exercise (Chapters 1 to 5) Part 2: Non-digestible carbohydrate, short-chain fatty acid production and skeletal muscle metabolism (Chapters 6 to 8) BACKGROUND Carbohydrate is the principal energy-contributing macronutrient in the typical human diet. Recent evidence has however suggested high intakes of dietary carbohydrate may increase disease and mortality risk, which has been coupled with a rapid increase in popularity of low-carbohydrate diets amongst the general population. Nevertheless, health-related claims regarding carbohydrate are often too simplistic as the term ‘carbohydrate’ constitutes a wide spectrum of foods that likely vary in their impact on human health. The sub-division of carbohydrate into various classifications can therefore provide a greater insight into the relationship between carbohydrate-containing foods and health. Carbohydrate can be classified as digestible or non-digestible depending on its capacity to be hydrolysed by host enzymes. Despite differences in the context in which digestible and non-digestible carbohydrate may benefit human health, both carbohydrate classes can influence the release of gastroenteropancreatic hormones and provide a substrate for skeletal muscle during exercise. The overall aim of this thesis was to investigate specific contexts in which digestible and non-digestible carbohydrate may provide benefit to human health, concentrating on their interaction with skeletal muscle, exercise, and gastroenteropancreatic hormone release. PART 1 Acute exercise is often accompanied by a temporary suppression of appetite referred to as ‘exercise-induced anorexia’. This response is often attributed to changes in glucagon-like peptide 1, peptide YY and acyl-ghrelin. However, acute exercise also influences the concentrations of other hormones that are implicated in appetite-regulation (the literature surrounding this topic area is reviewed in Chapter 1). In Chapter 2, the effect of acute exercise on glucose, insulin, and glucagon concentrations in the fed and fasted state was investigated using a systematic review and meta-analysis. Acute exercise resulted in decreased concentrations of glucose and insulin in the fed state, and increased glucagon concentrations irrespective of metabolic state. As raised systemic glucagon concentrations has previously been implicated in appetite suppression, these results suggested that glucagon may play a role in exercise-induced anorexia. Chapter 3 followed up the results of Chapter 2 by examining the effect of acute glucagon administration on subjective appetite and energy intake in humans via a systematic review and meta-analysis, identifying an inconsistent effect on appetite and energy intake. Therefore, the possible role of glucagon in exercise-induced anorexia could not be evaluated. Chapter 4 explored the independent and interactive effects of digestible carbohydrate and exercise on gastroenteropancreatic hormone release, and it is implications for appetite and energy balance. Digestible carbohydrate and exercise independently and interactively modulated the hormonal milieu and plasma metabolome, resulting in the generation of distinct metabolic phenotypes. GLP-1, acetate, lactate, and succinate were also identified as putative mediators of exercise-induced suppression of appetite and energy intake. However, no strong relationship between glucagon and exercise-induced appetite suppression or energy intake was found. A general discussion of the work presented in part 1 of this thesis is provided in Chapter 5. PART 2 Non-digestible carbohydrate, the majority of which constitutes dietary fibre, escapes digestion and is subsequently available for fermentation by resident colonic bacteria, resulting in the generation of metabolites such as short-chain fatty acids. Short-chain fatty acids can enter the systemic circulation where they can influence the metabolism and function of multiple organs, including skeletal muscle (the literature surrounding this topic area is reviewed in Chapter 6). Chapter 7 investigated the relationship between dietary fibre intake and skeletal muscle metabolism and function in a cohort at risk of skeletal muscle atrophy using a nationally representative dataset. Increased consumption of dietary fibre was associated with increased skeletal muscle mass and strength after adjusting for key confounders. A general discussion of the work presented in part 1 of this thesis is provided in Chapter 8. SUMMARY Overall, these studies demonstrate that glucagon is unlikely to play a role in exercise-induced anorexia despite acute exercise being a potent stimulator of glucagon release. These studies also identify acetate and succinate as novel regulators of exercise-induced changes in appetite and energy intake, and show that increasing dietary fibre is associated with higher relative skeletal muscle mass and strength.