The Effects of Macronutrient and Energy Availability on Metabolic Responses to Exercise: Implications for Training Adaptation
Traditional nutritional guidelines for endurance athletes typically advise high carbohydrate (CHO) availability before, during, and after exercise in order to support high training intensities and volumes. However, accumulating data now suggest that restricting CHO and/or energy availability around training may augment the exercise-induced cell signalling responses associated with oxidative adaptations in human skeletal muscle. In addition to the manipulation of CHO availability, there is also a growing interest in the role of increased dietary fat intakes in augmenting components of training adaptation. The aim of this thesis was to therefore assess the effects of macronutrient and energy availability on the regulation of molecular signalling pathways associated with mitochondrial biogenesis, lipid metabolism and muscle protein synthesis. A secondary aim was to also examine the acute effects of CHO and energy restriction on physiological markers associated with the syndrome of Relative Energy Deficiency in Sport (RED-S). Study 1 (Chapter 4) examined the effects of reduced CHO but high post-exercise fat availability on the activation of cell signalling kinases and expression of genes with roles in the regulation of mitochondrial biogenesis, lipid metabolism and muscle protein synthesis. In a repeated measures design, ten male participants completed a morning high intensity interval (HIT) running session (AM-HIT) followed by an afternoon steady state running session (PM-SS), under conditions of either high CHO (HCHO), or isocaloric low CHO but high fat (HFAT) availability in the post-exercise recovery period. Muscle glycogen was lower (P<0.05) at 3 (251 vs 301 mmol.kg-1dw) and 15 h (182 vs 312 mmol.kg-1dw) post afternoon exercise in HFAT compared to HCHO, however comparable increases (all P<0.05) in PGC-1α, p53, CS, Tfam, PPAR and ERRα mRNA were observed in HCHO and HFAT in response to exercise. AMPK-α2 activity was not increased post-exercise in either condition (P=0.41). HFAT induced greater increases in PDK4 (P=0.003), CD36 (P=0.05) and CPT1 (P=0.03) mRNA in the recovery period from afternoon exercise compared with HCHO. p70S6K activity was higher (P=0.08) at 3-h post-afternoon exercise in HCHO versus HFAT (72.7 ± 51.9 vs 44.7 ± 27 fmol.min-1 mg-1). Data demonstrate 1) that restricting CHO in the post-exercise recovery period has no further modulatory effect on the expression of genes associated with regulatory roles in mitochondrial biogenesis when overall energy availability is matched to a high CHO condition, and 2) high fat feeding may impair the regulation of muscle protein synthesis through reduced p70S6K signalling. Having identified that high dietary fat intake does not augment mitochondrial biogenesis related signalling, the aim of Study 2 (Chapter 5) was to examine the effects of both post-exercise CHO and caloric restriction on the modulation of such pathways. In a repeated-measures design, eight male participants completed a twice per day exercise model whereby two bouts of HIT running were completed in the morning (AM-HIT) and afternoon (PM-HIT). These sessions were completed under three different dietary conditions consisting of either high CHO availability (HCHO) in the recovery period after both training sessions, reduced CHO but high fat availability (LCHF), or finally reduced CHO and reduced energy intake (LCAL). Muscle glycogen was reduced to comparable levels (~200-250 mmol.kg-1 dw) in all trials immediately post PM-HIT and remained lower at 3-h (156, 182, and 345mmol.kg-1 dw, P< 0.001) and 15-h post-exercise (171, 194, and 316mmol.kg-1 dw, P< 0.001) in LCHF and LCAL compared to HCHO. Phosphorylation of p38MAPK increased (P=0.037) immediately post-exercise, though no differences existed between dietary conditions (P = 0.755). Comparable increases (all P < 0.05) in PGC-1α, p53, CPT1 and CD36 mRNA were observed in HCHO, LCHF and LCAL. In contrast, PDK4 mRNA expression (P = 0.004) was greater in LCHF and LCAL in the recovery period from PM-HIT compared to HCHO, whilst SIRT1 mRNA expression was also greater in LCAL compared to HCHO and LCHF. Data demonstrate that under conditions where muscle glycogen is maintained within the range of 200-350 mmol.kg-1 dw, short-term periods of acute CHO and energy restriction (i.e. <24-h) does not potentiate skeletal muscle signalling pathways associated with the regulation of mitochondrial biogenesis and lipid metabolism. Whilst the acute manipulations of CHO and energy availability did not likely achieve absolute glycogen concentrations sufficient to constitute “true” train-low conditions, it is possible that such alterations in dietary intake may regulate other aspects of physiological function, many of which are associated with symptoms of RED-S. As such, Study 3 (Chapter 6) examined the effects of post-exercise CHO restriction and caloric restriction on markers of bone turnover, inflammation and appetite regulation. In an identical study design to Study 2 (Chapter 5), nine male participants exercised under three dietary conditions consisting of either high CHO availability (HCHO) in the recovery period after both training sessions, reduced CHO but high fat availability (LCHF), or finally reduced CHO and reduced energy intake (LCAL). Bone breakdown marker βCTX responses were significantly lower across all time points in the post-exercise period in HCHO (P=0.035) compared to LCHF and LCAL. Both AM-HIT (P=0.001) and PM-HIT (P=0.005) significantly increased bone formation marker P1NP responses but there was no difference between trials (P=0.633). IL-6 responses to exercise were higher in LCAL (P = 0.016) post PM-HIT compared to LCHF and HCHO. Circulating leptin levels were significantly lower (P = 0.04) in LCAL compared to HCHO in the post exercise sampling period. There was no difference in the short-term response of ghrelin to feeding (P= 0.408) with increases following both AM-HIT (P = 0.001) and PM-HIT (P = 0.025) in all three trials. Data demonstrate that consuming CHO before, during and after HIT running attenuates circulating β-CTX concentrations in the hours after exercise, effects that are independent of energy availability. In contrast, energy availability (but not CHO availability) modulates the regulation of post-exercise circulating leptin and IL-6 concentrations. In summary, we provide novel data by demonstrating that in conditions where post-exercise muscle glycogen concentration is maintained within the range of 200-350 mmol.kg-1 dw, short-term periods of acute CHO and energy restriction (i.e. <24 hours) does not potentiate skeletal muscle signalling pathways associated with the regulation of mitochondrial biogenesis and lipid metabolism. In addition, promotion of high CHO availability before, during and in recovery from exercise appears to be of greater importance for the acute regulation of bone turnover when compared with energy intake per se. In contrast, energy availability appears a more influential factor in regulating both IL-6 and leptin responses in recovery from exercise as opposed to CHO availability per se. Future studies should now examine the potential presence of a muscle glycogen threshold as an important regulator of skeletal muscle adaptations to endurance training. Additionally, the long-term implications (in relation to RED-S) of the acute within day fluctuations in both CHO and energy availability that occur when training twice per day should now be examined when performed as part of a periodised training programme.
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