1932

Abstract

Focusing on daily nutrition is important for athletes to perform and adapt optimally to exercise training. The major roles of an athlete's daily diet are to supply the substrates needed to cover the energy demands for exercise, to ensure quick recovery between exercise bouts, to optimize adaptations to exercise training, and to stay healthy. The major energy substrates for exercising skeletal muscles are carbohydrate and fat stores. Optimizing the timing and type of energy intake and the amount of dietary macronutrients is essential to ensure peak training and competition performance, and these strategies play important roles in modulating skeletal muscle adaptations to endurance and resistance training. In this review, recent advances in nutritional strategies designed to optimize exercise-induced adaptations in skeletal muscle are discussed, with an emphasis on mechanistic approaches, by describing the physiological mechanisms that provide the basis for different nutrition regimens.

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2019-08-21
2024-06-22
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Literature Cited

  1. 1.
    Alghannam AF, Jedrzejewski D, Tweddle MG, Gribble H, Bilzon J et al. 2016. Impact of muscle glycogen availability on the capacity for repeated exercise in man. Med. Sci. Sports Exerc. 48:123–31
    [Google Scholar]
  2. 2.
    Anthony JC, Anthony TG, Layman DK 1999. Leucine supplementation enhances skeletal muscle recovery in rats following exercise. J. Nutr. 129:1102–6
    [Google Scholar]
  3. 3.
    Antonio J, Ellerbroek A, Silver T, Orris S, Scheiner M et al. 2015. A high protein diet (3.4 g/kg/d) combined with a heavy resistance training program improves body composition in healthy trained men and women—a follow-up investigation. J. Int. Soc. Sports Nutr. 12:39
    [Google Scholar]
  4. 4.
    Aragon AA, Schoenfeld BJ. 2013. Nutrient timing revisited: Is there a post-exercise anabolic window?. J. Int. Soc. Sports Nutr. 10:5–10
    [Google Scholar]
  5. 5.
    Areta JL, Burke LM, Ross ML, Camera DM, West DW et al. 2013. Timing and distribution of protein ingestion during prolonged recovery from resistance exercise alters myofibrillar protein synthesis. J. Physiol. 591:2319–31
    [Google Scholar]
  6. 6.
    Asp S, Daugaard JR, Kristiansen S, Kiens B, Richter EA 1996. Eccentric exercise decreases maximal insulin action in humans: muscle and systemic effects. J. Physiol. 494:891–98
    [Google Scholar]
  7. 7.
    Atherton PJ, Etheridge T, Watt PW, Wilkinson D, Selby A et al. 2010. Muscle full effect after oral protein: time-dependent concordance and discordance between human muscle protein synthesis and mTORC1 signaling. Am. J. Clin. Nutr. 92:1080–88
    [Google Scholar]
  8. 8.
    Balasse EO, Fery F. 1989. Ketone body production and disposal: effects of fasting, diabetes, and exercise. Diabetes Metab. Rev. 5:247–70
    [Google Scholar]
  9. 9.
    Basu R, Di CB, Toffolo G, Basu A, Shah P et al. 2003. Use of a novel triple-tracer approach to assess postprandial glucose metabolism. Am. J. Physiol. Endocrinol. Metab. 284:E55–69
    [Google Scholar]
  10. 10.
    Bergman BC, Butterfield GE, Wolfel EE, Lopaschuk GD, Casazza GA et al. 1999. Muscle net glucose uptake and glucose kinetics after endurance training in men. Am. J. Physiol. 277:E81–92
    [Google Scholar]
  11. 11.
    Bergstrom J, Hultman E. 1967. Synthesis of muscle glycogen in man after glucose and fructose infusion. Acta Med. Scand. 182:93–107
    [Google Scholar]
  12. 12.
    Biolo G, Williams BD, Fleming RY, Wolfe RR 1999. Insulin action on muscle protein kinetics and amino acid transport during recovery after resistance exercise. Diabetes 48:949–57
    [Google Scholar]
  13. 13.
    Blom CS. 1989. Post-exercise glucose uptake and glycogen synthesis in human muscle during oral or IV glucose intake. Eur. J. Appl. Physiol. Occup. Physiol. 59:327–33
    [Google Scholar]
  14. 14.
    Blom PC, Hostmark AT, Vaage O, Kardel KR, Maehlum S 1987. Effect of different post-exercise sugar diets on the rate of muscle glycogen synthesis. Med. Sci. Sports Exerc. 19:491–96
    [Google Scholar]
  15. 15.
    Bohe J, Low A, Wolfe RR, Rennie MJ 2003. Human muscle protein synthesis is modulated by extracellular, not intramuscular, amino acid availability: a dose–response study. J. Physiol. 552:315–24
    [Google Scholar]
  16. 16.
    Borsheim E, Tipton KD, Wolf SE, Wolfe RR 2002. Essential amino acids and muscle protein recovery from resistance exercise. Am. J. Physiol. Endocrinol. Metab. 283:E648–57
    [Google Scholar]
  17. 17.
    Breen L, Philp A, Witard OC, Jackman SR, Selby A et al. 2011. The influence of carbohydrate–protein co-ingestion following endurance exercise on myofibrillar and mitochondrial protein synthesis. J. Physiol. 589:4011–25
    [Google Scholar]
  18. 18.
    Burd NA, Gorissen SH, van Vliet S, Snijders T, van Loon LJ 2015. Differences in postprandial protein handling after beef compared with milk ingestion during postexercise recovery: a randomized controlled trial. Am. J. Clin. Nutr. 102:828–36
    [Google Scholar]
  19. 19.
    Burd NA, West DW, Moore DR, Atherton PJ, Staples AW et al. 2011. Enhanced amino acid sensitivity of myofibrillar protein synthesis persists for up to 24 h after resistance exercise in young men. J. Nutr. 141:568–73
    [Google Scholar]
  20. 20.
    Burke DG, Chilibeck PD, Davidson KS, Candow DG, Farthing J, Smith-Palmer T 2001. The effect of whey protein supplementation with and without creatine monohydrate combined with resistance training on lean tissue mass and muscle strength. Int. J. Sport Nutr. Exerc. Metab. 11:349–64
    [Google Scholar]
  21. 21.
    Burke LM. 2015. Re-examining high-fat diets for sports performance: Did we call the ‘nail in the coffin’ too soon?. Sports Med 45:Suppl. 1S33–49
    [Google Scholar]
  22. 22.
    Burke LM, Angus DJ, Cox GR, Cummings NK, Febbraio MA et al. 2000. Effect of fat adaptation and carbohydrate restoration on metabolism and performance during prolonged cycling. J. Appl. Physiol. 89:2413–21
    [Google Scholar]
  23. 23.
    Burke LM, Collier GR, Hargreaves M 1993. Muscle glycogen storage after prolonged exercise: effect of the glycemic index of carbohydrate feedings. J. Appl. Physiol. 75:1019–23
    [Google Scholar]
  24. 24.
    Burke LM, Kiens B, Ivy JL 2004. Carbohydrates and fat for training and recovery. J. Sports Sci. 22:15–30
    [Google Scholar]
  25. 25.
    Burke LM, Ross ML, Garvican-Lewis LA, Welvaert M, Heikura IA et al. 2017. Low carbohydrate, high fat diet impairs exercise economy and negates the performance benefit from intensified training in elite race walkers. J. Physiol. 595:2785–807
    [Google Scholar]
  26. 26.
    Butterfield GE, Calloway DH. 1984. Physical activity improves protein utilization in young men. Br. J. Nutr. 51:171–84
    [Google Scholar]
  27. 27.
    Cameron-Smith D, Burke LM, Angus DJ, Tunstall RJ, Cox GR et al. 2003. A short-term, high-fat diet up-regulates lipid metabolism and gene expression in human skeletal muscle. Am. J. Clin. Nutr. 77:313–18
    [Google Scholar]
  28. 28.
    Carrithers JA, Williamson DL, Gallagher PM, Godard MP, Schulze KE, Trappe SW 2000. Effects of postexercise carbohydrate–protein feedings on muscle glycogen restoration. J. Appl. Physiol. 88:1976–82
    [Google Scholar]
  29. 29.
    Casey A, Mann R, Banister K, Fox J, Morris PG et al. 2000. Effect of carbohydrate ingestion on glycogen resynthesis in human liver and skeletal muscle, measured by 13C MRS. Am. J. Physiol. Endocrinol. Metab. 278:E65–75
    [Google Scholar]
  30. 30.
    Casey A, Short AH, Hultman E, Greenhaff PL 1995. Glycogen resynthesis in human muscle fibre types following exercise-induced glycogen depletion. J. Physiol. 483:265–71
    [Google Scholar]
  31. 31.
    Cermak NM, Res PT, de Groot LC, Saris WH, van Loon LJ 2012. Protein supplementation augments the adaptive response of skeletal muscle to resistance-type exercise training: a meta-analysis. Am. J. Clin. Nutr. 96:1454–64
    [Google Scholar]
  32. 32.
    Churchward-Venne TA, Breen L, Di Donato DM, Hector AJ, Mitchell CJ et al. 2014. Leucine supplementation of a low-protein mixed macronutrient beverage enhances myofibrillar protein synthesis in young men: a double-blind, randomized trial. Am. J. Clin. Nutr. 99:276–86
    [Google Scholar]
  33. 33.
    Churchward-Venne TA, Burd NA, Mitchell CJ, West DW, Philp A et al. 2012. Supplementation of a suboptimal protein dose with leucine or essential amino acids: effects on myofibrillar protein synthesis at rest and following resistance exercise in men. J. Physiol. 590:2751–65
    [Google Scholar]
  34. 34.
    Coffey VG, Moore DR, Burd NA, Rerecich T, Stellingwerff T et al. 2011. Nutrient provision increases signalling and protein synthesis in human skeletal muscle after repeated sprints. Eur. J. Appl. Physiol. 111:1473–83
    [Google Scholar]
  35. 35.
    Cox PJ, Kirk T, Ashmore T, Willerton K, Evans R et al. 2016. Nutritional ketosis alters fuel preference and thereby endurance performance in athletes. Cell Metab 24:256–68
    [Google Scholar]
  36. 36.
    Crapo PA, Kolterman OG, Olefsky JM 1980. Effects of oral fructose in normal, diabetic, and impaired glucose tolerance subjects. Diabetes Care 3:575–82
    [Google Scholar]
  37. 37.
    Cribb PJ, Hayes A. 2006. Effects of supplement timing and resistance exercise on skeletal muscle hypertrophy. Med. Sci. Sports Exerc. 38:1918–25
    [Google Scholar]
  38. 38.
    De Bock K, Derave W, Eijnde BO, Hesselink MK, Koninckx E et al. 2008. Effect of training in the fasted state on metabolic responses during exercise with carbohydrate intake. J. Appl. Physiol. 104:1045–55
    [Google Scholar]
  39. 39.
    Doyle JA, Sherman WM, Strauss RL 1993. Effects of eccentric and concentric exercise on muscle glycogen replenishment. J. Appl. Physiol. 74:1848–55
    [Google Scholar]
  40. 40.
    Elliot TA, Cree MG, Sanford AP, Wolfe RR, Tipton KD 2006. Milk ingestion stimulates net muscle protein synthesis following resistance exercise. Med. Sci. Sports Exerc. 38:667–74
    [Google Scholar]
  41. 41.
    Fery F, Balasse EO. 1986. Response of ketone body metabolism to exercise during transition from postabsorptive to fasted state. Am. J. Physiol. 250:E495–501
    [Google Scholar]
  42. 42.
    Fritzen AM, Madsen AB, Kleinert M, Treebak JT, Lundsgaard AM et al. 2016. Regulation of autophagy in human skeletal muscle: effects of exercise, exercise training and insulin stimulation. J. Physiol. 594:745–61
    [Google Scholar]
  43. 43.
    Frøsig C, Rose AJ, Treebak JT, Kiens B, Richter EA, Wojtaszewski JF 2007. Effects of endurance exercise training on insulin signaling in human skeletal muscle: interactions at the level of phosphatidylinositol 3-kinase, Akt, and AS160. Diabetes 56:2093–102
    [Google Scholar]
  44. 44.
    Goedecke JH, Christie C, Wilson G, Dennis SC, Noakes TD et al. 1999. Metabolic adaptations to a high-fat diet in endurance cyclists. Metabolism 48:1509–17
    [Google Scholar]
  45. 45.
    Gollnick PD, Piehl K, Saltin B 1974. Selective glycogen depletion pattern in human muscle fibres after exercise of varying intensity and at varying pedalling rates. J. Physiol. 241:45–57
    [Google Scholar]
  46. 46.
    Gontzea I, Sutzescu P, Dumitrache S 1975. Influence of adaptation to physical effort on nitrogen balance in man. Nutr. Rep. Int. 22:231–36
    [Google Scholar]
  47. 47.
    Gonzalez JT, Fuchs CJ, Betts JA, van Loon LJ 2017. Glucose plus fructose ingestion for post-exercise recovery—greater than the sum of its parts?. Nutrients 9:344
    [Google Scholar]
  48. 48.
    Gregersen S, Samocha-Bonet D, Heilbronn LK, Campbell LV 2012. Inflammatory and oxidative stress responses to high-carbohydrate and high-fat meals in healthy humans. J. Nutr. Metab. 2012:238056
    [Google Scholar]
  49. 49.
    Groen BBL, Horstman AM, Hamer HM, de Haan M, van Kranenburg J et al. 2015. Post-prandial protein handling: You are what you just ate. PLOS ONE 10:e0141582
    [Google Scholar]
  50. 50.
    Hansen AK, Fischer CP, Plomgaard P, Andersen JL, Saltin B, Pedersen BK 2005. Skeletal muscle adaptation: training twice every second day versus training once daily. J. Appl. Physiol. 98:93–99
    [Google Scholar]
  51. 51.
    Hansen BF, Asp S, Kiens B, Richter EA 1999. Glycogen concentration in human skeletal muscle: effect of prolonged insulin and glucose infusion. Scand. J. Med. Sci. Sports 9:209–13
    [Google Scholar]
  52. 52.
    Hansen PA, Nolte LA, Chen MM, Holloszy JO 1998. Increased GLUT-4 translocation mediates enhanced insulin sensitivity of muscle glucose transport after exercise. J. Appl. Physiol. 85:1218–22
    [Google Scholar]
  53. 53.
    Hartman JW, Moore DR, Phillips SM 2006. Resistance training reduces whole-body protein turnover and improves net protein retention in untrained young males. Appl. Physiol. Nutr. Metab. 31:557–64
    [Google Scholar]
  54. 54.
    Hartman JW, Tang JE, Wilkinson SB, Tarnopolsky MA, Lawrence RL et al. 2007. Consumption of fat-free fluid milk after resistance exercise promotes greater lean mass accretion than does consumption of soy or carbohydrate in young, novice, male weightlifters. Am. J. Clin. Nutr. 86:373–81
    [Google Scholar]
  55. 55.
    Havemann L, West SJ, Goedecke JH, Macdonald IA, St. Clair GA et al. 2006. Fat adaptation followed by carbohydrate loading compromises high-intensity sprint performance. J. Appl. Physiol. 100:194–202
    [Google Scholar]
  56. 56.
    Helge JW, Kiens B. 1997. Muscle enzyme activity in humans: role of substrate availability and training. Am. J. Physiol. 272:R1620–24
    [Google Scholar]
  57. 57.
    Helge JW, Richter EA, Kiens B 1996. Interaction of training and diet on metabolism and endurance during exercise in man. J. Physiol. 492:293–306
    [Google Scholar]
  58. 58.
    Helge JW, Watt PW, Richter EA, Rennie MJ, Kiens B 2001. Fat utilization during exercise: adaptation to a fat-rich diet increases utilization of plasma fatty acids and very low density lipoprotein-triacylglycerol in humans. J. Physiol. 537:1009–20
    [Google Scholar]
  59. 59.
    Helge JW, Watt PW, Richter EA, Rennie MJ, Kiens B 2002. Partial restoration of dietary fat induced metabolic adaptations to training by 7 days of carbohydrate diet. J. Appl. Physiol. 93:1797–805
    [Google Scholar]
  60. 60.
    Helge JW, Wulff B, Kiens B 1998. Impact of a fat-rich diet on endurance in man: role of the dietary period. Med. Sci. Sports Exerc. 30:456–61
    [Google Scholar]
  61. 61.
    Henríquez-Olguín C, Renani LB, Arab-Ceschia L, Raun SH, Bhatia A et al. 2019. Adaptations to high-intensity interval training in skeletal muscle require NADPH oxidase 2. Redox Biol 24:101188
    [Google Scholar]
  62. 62.
    Hickner RC, Fisher JS, Hansen PA, Racette SB, Mier CM et al. 1997. Muscle glycogen accumulation after endurance exercise in trained and untrained individuals. J. Appl. Physiol. 83:897–903
    [Google Scholar]
  63. 63.
    Hoffman JR, Ratamess NA, Tranchina CP, Rashti SL, Kang J, Faigenbaum AD 2009. Effect of protein-supplement timing on strength, power, and body-composition changes in resistance-trained men. Int. J. Sport Nutr. Exerc. Metab. 19:172–85
    [Google Scholar]
  64. 64.
    Holway FE, Spriet LL. 2011. Sport-specific nutrition: practical strategies for team sports. J. Sports Sci. 29:Suppl. 1S115–25
    [Google Scholar]
  65. 65.
    Horvath PJ, Eagen CK, Ryer-Calvin SD, Pendergast DR 2000. The effects of varying dietary fat on the nutrient intake in male and female runners. J. Am. Coll. Nutr. 19:42–51
    [Google Scholar]
  66. 66.
    Howarth KR, Moreau NA, Phillips SM, Gibala MJ 2009. Coingestion of protein with carbohydrate during recovery from endurance exercise stimulates skeletal muscle protein synthesis in humans. J. Appl. Physiol. 106:1394–402
    [Google Scholar]
  67. 67.
    Hulston CJ, Venables MC, Mann CH, Martin C, Philp A et al. 2010. Training with low muscle glycogen enhances fat metabolism in well-trained cyclists. Med. Sci. Sports Exerc. 42:2046–55
    [Google Scholar]
  68. 68.
    Impey SG, Hammond KM, Shepherd SO, Sharples AP, Stewart C et al. 2016. Fuel for the work required: a practical approach to amalgamating train-low paradigms for endurance athletes. Physiol. Rep. 4:e12803
    [Google Scholar]
  69. 69.
    Ivy JL, Katz AL, Cutler CL, Sherman WM, Coyle EF 1988. Muscle glycogen synthesis after exercise: effect of time of carbohydrate ingestion. J. Appl. Physiol. 64:1480–85
    [Google Scholar]
  70. 70.
    Ivy JL, Lee MC, Brozinick JT Jr, Reed MJ 1988. Muscle glycogen storage after different amounts of carbohydrate ingestion. J. Appl. Physiol. 65:2018–23
    [Google Scholar]
  71. 71.
    Jager R, Kerksick CM, Campbell BI, Cribb PJ, Wells SD et al. 2017. International Society of Sports Nutrition Position Stand: protein and exercise. J. Int. Soc. Sports Nutr. 14:20
    [Google Scholar]
  72. 72.
    Jain SS, Paglialunga S, Vigna C, Ludzki A, Herbst EA et al. 2014. High-fat diet-induced mitochondrial biogenesis is regulated by mitochondrial-derived reactive oxygen species activation of CaMKII. Diabetes 63:1907–13
    [Google Scholar]
  73. 73.
    Jensen L, Gejl KD, Ortenblad N, Nielsen JL, Bech RD et al. 2015. Carbohydrate restricted recovery from long term endurance exercise does not affect gene responses involved in mitochondrial biogenesis in highly trained athletes. Physiol. Rep. 3:e12184
    [Google Scholar]
  74. 74.
    Jentjens RL, van Loon LJ, Mann CH, Wagenmakers AJ, Jeukendrup AE 2001. Addition of protein and amino acids to carbohydrates does not enhance postexercise muscle glycogen synthesis. J. Appl. Physiol. 91:839–46
    [Google Scholar]
  75. 75.
    Jordy AB, Kiens B. 2014. Regulation of exercise-induced lipid metabolism in skeletal muscle. Exp. Physiol. 99:1586–92
    [Google Scholar]
  76. 76.
    Joy JM, Lowery RP, Wilson JM, Purpura M, De Souza EO et al. 2013. The effects of 8 weeks of whey or rice protein supplementation on body composition and exercise performance. Nutr. J. 12:86
    [Google Scholar]
  77. 77.
    Kato H, Suzuki K, Bannai M, Moore DR 2016. Protein requirements are elevated in endurance athletes after exercise as determined by the indicator amino acid oxidation method. PLOS ONE 11:e0157406
    [Google Scholar]
  78. 78.
    Kiens B, Helge JW. 1998. Effect of high-fat diets on exercise performance. Proc. Nutr. Soc. 57:73–75
    [Google Scholar]
  79. 79.
    Kiens B, Richter EA. 1998. Utilization of skeletal muscle triacylglycerol during postexercise recovery in humans. Am. J. Physiol. 275:E332–37
    [Google Scholar]
  80. 80.
    Kim IY, Deutz NEP, Wolfe RR 2018. Update on maximal anabolic response to dietary protein. Clin. Nutr. 37:411–18
    [Google Scholar]
  81. 81.
    Kim IY, Schutzler S, Schrader A, Spencer HJ, Azhar G et al. 2016. The anabolic response to a meal containing different amounts of protein is not limited by the maximal stimulation of protein synthesis in healthy young adults. Am. J. Physiol. Endocrinol. Metab 310:E73–80
    [Google Scholar]
  82. 82.
    Kim IY, Schutzler S, Schrader A, Spencer HJ, Kortebein P et al. 2015. Quantity of dietary protein intake, but not pattern of intake, affects net protein balance primarily through differences in protein synthesis in older adults. Am. J. Physiol. Endocrinol. Metab 308:E21–28
    [Google Scholar]
  83. 83.
    Kim PL, Staron RS, Phillips SM 2005. Fasted-state skeletal muscle protein synthesis after resistance exercise is altered with training. J. Physiol. 568:283–90
    [Google Scholar]
  84. 84.
    Kleinert M, Parker BL, Jensen TE, Raun SH, Pham P et al. 2018. Quantitative proteomic characterization of cellular pathways associated with altered insulin sensitivity in skeletal muscle following high-fat diet feeding and exercise training. Sci. Rep. 8:10723
    [Google Scholar]
  85. 85.
    Lamont LS, Patel DG, Kalhan SC 1990. Leucine kinetics in endurance-trained humans. J. Appl. Physiol. 69:1–6
    [Google Scholar]
  86. 86.
    Leckey JJ, Hoffman NJ, Parr EB, Devlin BL, Trewin AJ et al. 2018. High dietary fat intake increases fat oxidation and reduces skeletal muscle mitochondrial respiration in trained humans. FASEB J 32:2979–91
    [Google Scholar]
  87. 87.
    Leckey JJ, Ross ML, Quod M, Hawley JA, Burke LM 2017. Ketone diester ingestion impairs time-trial performance in professional cyclists. Front. Physiol. 8:806
    [Google Scholar]
  88. 88.
    Levenhagen DK, Carr C, Carlson MG, Maron DJ, Borel MJ, Flakoll PJ 2002. Postexercise protein intake enhances whole-body and leg protein accretion in humans. Med. Sci. Sports Exerc. 34:828–37
    [Google Scholar]
  89. 89.
    Levenhagen DK, Gresham JD, Carlson MG, Maron DJ, Borel MJ, Flakoll PJ 2001. Postexercise nutrient intake timing in humans is critical to recovery of leg glucose and protein homeostasis. Am. J. Physiol. Endocrinol. Metab. 280:E982–93
    [Google Scholar]
  90. 90.
    Long CL, Birkhahn RH, Geiger JW, Blakemore WS 1981. Contribution of skeletal muscle protein in elevated rates of whole body protein catabolism in trauma patients. Am. J. Clin. Nutr. 34:1087–93
    [Google Scholar]
  91. 91.
    Lundsgaard AM, Fritzen AM, Kiens B 2018. Molecular regulation of fatty acid oxidation in skeletal muscle during aerobic exercise. Trends Endocrinol. Metab. 29:18–30
    [Google Scholar]
  92. 92.
    Lundsgaard AM, Holm JB, Sjøberg KA, Bojsen-Møller KN, Myrmel LS et al. 2019. Mechanisms preserving insulin action during high dietary fat intake. Cell Metab 29:50–63.e4
    [Google Scholar]
  93. 93.
    Lundsgaard AM, Sjøberg KA, Høeg LD, Jeppesen J, Jordy AB et al. 2017. Opposite regulation of insulin sensitivity by dietary lipid versus carbohydrate excess. Diabetes 66:2583–95
    [Google Scholar]
  94. 94.
    Macnaughton LS, Wardle SL, Witard OC, McGlory C, Hamilton DL et al. 2016. The response of muscle protein synthesis following whole-body resistance exercise is greater following 40 g than 20 g of ingested whey protein. Physiol. Rep. 4:e12893
    [Google Scholar]
  95. 95.
    Maehlum S, Grandmontagne M, Newsholme EA, Sejersted OM 1986. Magnitude and duration of excess postexercise oxygen consumption in healthy young subjects. Metabolism 35:425–29
    [Google Scholar]
  96. 96.
    Mayhew DL, Kim JS, Cross JM, Ferrando AA, Bamman MM 2009. Translational signaling responses preceding resistance training–mediated myofiber hypertrophy in young and old humans. J. Appl. Physiol. 107:1655–62
    [Google Scholar]
  97. 97.
    McCoy M, Proietto J, Hargreaves M 1996. Skeletal muscle GLUT-4 and postexercise muscle glycogen storage in humans. J. Appl. Physiol. 80:411–15
    [Google Scholar]
  98. 98.
    McKenzie S, Phillips SM, Carter SL, Lowther S, Gibala MJ, Tarnopolsky MA 2000. Endurance exercise training attenuates leucine oxidation and BCOAD activation during exercise in humans. Am. J. Physiol. Endocrinol. Metab 278:E580–87
    [Google Scholar]
  99. 99.
    McSwiney FT, Wardrop B, Hyde PN, Lafountain RA, Volek JS, Doyle L 2018. Keto-adaptation enhances exercise performance and body composition responses to training in endurance athletes. Metabolism 81:25–34
    [Google Scholar]
  100. 100.
    Mikkelsen KH, Seifert T, Secher NH, Grondal T, van Hall G 2015. Systemic, cerebral and skeletal muscle ketone body and energy metabolism during acute hyper-D-β-hydroxybutyratemia in post-absorptive healthy males. J. Clin. Endocrinol. Metab. 100:636–43
    [Google Scholar]
  101. 101.
    Millward DJ. 2001. Methodological considerations. Proc. Nutr. Soc. 60:3–5
    [Google Scholar]
  102. 102.
    Mitchell CJ, Churchward-Venne TA, Parise G, Bellamy L, Baker SK et al. 2014. Acute post-exercise myofibrillar protein synthesis is not correlated with resistance training–induced muscle hypertrophy in young men. PLOS ONE 9:e89431
    [Google Scholar]
  103. 103.
    Moore DR, Churchward-Venne TA, Witard O, Breen L, Burd NA et al. 2015. Protein ingestion to stimulate myofibrillar protein synthesis requires greater relative protein intakes in healthy older versus younger men. J. Gerontol. A 70:57–62
    [Google Scholar]
  104. 104.
    Moore DR, Robinson MJ, Fry JL, Tang JE, Glover EI et al. 2009. Ingested protein dose response of muscle and albumin protein synthesis after resistance exercise in young men. Am. J. Clin. Nutr. 89:161–68
    [Google Scholar]
  105. 105.
    Morrison DJ, Kowalski GM, Grespan E, Mari A, Bruce CR, Wadley GD 2018. Measurement of postprandial glucose fluxes in response to acute and chronic endurance exercise in healthy humans. Am. J. Physiol. Endocrinol. Metab. 314:E503–11
    [Google Scholar]
  106. 106.
    Morton RW, Murphy KT, McKellar SR, Schoenfeld BJ, Henselmans M et al. 2018. A systematic review, meta-analysis and meta-regression of the effect of protein supplementation on resistance training–induced gains in muscle mass and strength in healthy adults. Br. J. Sports Med. 52:376–84
    [Google Scholar]
  107. 107.
    Parkin JA, Carey MF, Martin IK, Stojanovska L, Febbraio MA 1997. Muscle glycogen storage following prolonged exercise: effect of timing of ingestion of high glycemic index food. Med. Sci. Sports Exerc. 29:220–24
    [Google Scholar]
  108. 108.
    Pencek RR, James F, Lacy DB, Jabbour K, Williams PE et al. 2003. Interaction of insulin and prior exercise in control of hepatic metabolism of a glucose load. Diabetes 52:1897–903
    [Google Scholar]
  109. 109.
    Petersen KF, Price TB, Bergeron R 2004. Regulation of net hepatic glycogenolysis and gluconeogenesis during exercise: impact of type 1 diabetes. J. Clin. Endocrinol. Metab. 89:4656–64
    [Google Scholar]
  110. 110.
    Phillips SM. 2004. Protein requirements and supplementation in strength sports. Nutrition 20:689–95
    [Google Scholar]
  111. 111.
    Phillips SM, Fulgoni VL III, Heaney RP, Nicklas TA, Slavin JL, Weaver CM 2015. Commonly consumed protein foods contribute to nutrient intake, diet quality, and nutrient adequacy. Am. J. Clin. Nutr. 101:1346S–52S
    [Google Scholar]
  112. 112.
    Philp A, Schenk S, Perez-Schindler J, Hamilton DL, Breen L et al. 2015. Rapamycin does not prevent increases in myofibrillar or mitochondrial protein synthesis following endurance exercise. J. Physiol. 593:4275–84
    [Google Scholar]
  113. 113.
    Piehl AK, Soderlund K, Hultman E 2000. Muscle glycogen resynthesis rate in humans after supplementation of drinks containing carbohydrates with low and high molecular masses. Eur. J. Appl. Physiol. 81:346–51
    [Google Scholar]
  114. 114.
    Pilegaard H, Keller C, Steensberg A, Helge JW, Pedersen BK et al. 2002. Influence of pre-exercise muscle glycogen content on exercise-induced transcriptional regulation of metabolic genes. J. Physiol. 541:261–71
    [Google Scholar]
  115. 115.
    Pinho RA, Sepa-Kishi DM, Bikopoulos G, Wu MV, Uthayakumar A et al. 2017. High-fat diet induces skeletal muscle oxidative stress in a fiber type–dependent manner in rats. Free Radic. Biol. Med. 110:381–89
    [Google Scholar]
  116. 116.
    Powers SK, Jackson MJ. 2008. Exercise-induced oxidative stress: cellular mechanisms and impact on muscle force production. Physiol. Rev. 88:1243–76
    [Google Scholar]
  117. 117.
    Psilander N, Frank P, Flockhart M, Sahlin K 2013. Exercise with low glycogen increases PGC-1α gene expression in human skeletal muscle. Eur. J. Appl. Physiol. 113:951–63
    [Google Scholar]
  118. 118.
    Rasmussen BB, Tipton KD, Miller SL, Wolf SE, Wolfe RR 2000. An oral essential amino acid–carbohydrate supplement enhances muscle protein anabolism after resistance exercise. J. Appl. Physiol. 88:386–92
    [Google Scholar]
  119. 119.
    Reed MJ, Brozinick JT Jr, Lee MC, Ivy JL 1989. Muscle glycogen storage postexercise: effect of mode of carbohydrate administration. J. Appl. Physiol 66:720–26
    [Google Scholar]
  120. 120.
    Reidy PT, Walker DK, Dickinson JM, Gundermann DM, Drummond MJ et al. 2013. Protein blend ingestion following resistance exercise promotes human muscle protein synthesis. J. Nutr. 143:410–16
    [Google Scholar]
  121. 121.
    Res PT, Groen B, Pennings B, Beelen M, Wallis GA et al. 2012. Protein ingestion before sleep improves postexercise overnight recovery. Med. Sci. Sports Exerc. 44:1560–69
    [Google Scholar]
  122. 122.
    Rose AJ, Howlett K, King DS, Hargreaves M 2001. Effect of prior exercise on glucose metabolism in trained men. Am. J. Physiol. Endocrinol. Metab. 281:E766–71
    [Google Scholar]
  123. 123.
    Rothman DL, Magnusson I, Katz LD, Shulman RG, Shulman GI 1991. Quantitation of hepatic glycogenolysis and gluconeogenesis in fasting humans with 13C NMR. Science 254:573–76
    [Google Scholar]
  124. 124.
    Rowlands DS, Nelson AR, Phillips SM, Faulkner JA, Clarke J et al. 2015. Protein–leucine fed dose effects on muscle protein synthesis after endurance exercise. Med. Sci. Sports Exerc. 47:547–55
    [Google Scholar]
  125. 125.
    Schoenfeld BJ, Aragon AA, Krieger JW 2013. The effect of protein timing on muscle strength and hypertrophy: a meta-analysis. J. Int. Soc. Sports Nutr. 10:53
    [Google Scholar]
  126. 126.
    Sjøberg KA, Frøsig C, Kjøbsted R, Sylow L, Kleinert M et al. 2017. Exercise increases human skeletal muscle insulin sensitivity via coordinated increases in microvascular perfusion and molecular signaling. Diabetes 66:1501–10
    [Google Scholar]
  127. 127.
    Slater G, Phillips SM. 2011. Nutrition guidelines for strength sports: sprinting, weightlifting, throwing events, and bodybuilding. J. Sports Sci. 29:Suppl. 1S67–77
    [Google Scholar]
  128. 128.
    Snijders T, Res PT, Smeets JS, van Vliet S, van Kranenburg J et al. 2015. Protein ingestion before sleep increases muscle mass and strength gains during prolonged resistance-type exercise training in healthy young men. J. Nutr. 145:1178–84
    [Google Scholar]
  129. 129.
    Steinberg GR, Watt MJ, McGee SL, Chan S, Hargreaves M et al. 2006. Reduced glycogen availability is associated with increased AMPKα2 activity, nuclear AMPKα2 protein abundance, and GLUT4 mRNA expression in contracting human skeletal muscle. Appl. Physiol. Nutr. Metab. 31:302–12
    [Google Scholar]
  130. 130.
    Stellingwerff T, Spriet LL, Watt MJ, Kimber NE, Hargreaves M et al. 2006. Decreased PDH activation and glycogenolysis during exercise following fat adaptation with carbohydrate restoration. Am. J. Physiol. Endocrinol. Metab 290:E380–88
    [Google Scholar]
  131. 131.
    Stoll B, Henry J, Reeds PJ, Yu H, Jahoor F, Burrin DG 1998. Catabolism dominates the first-pass intestinal metabolism of dietary essential amino acids in milk protein–fed piglets. J. Nutr. 128:606–14
    [Google Scholar]
  132. 132.
    Stubbs BJ, Cox PJ, Evans RD, Cyranka M, Clarke K, de Wet H 2018. A ketone ester drink lowers human ghrelin and appetite. Obesity 26:269–73
    [Google Scholar]
  133. 133.
    Stubbs BJ, Cox PJ, Evans RD, Santer P, Miller JJ et al. 2017. On the metabolism of exogenous ketones in humans. Front. Physiol. 8:848
    [Google Scholar]
  134. 134.
    Symons TB, Sheffield-Moore M, Wolfe RR, Paddon-Jones D 2009. A moderate serving of high-quality protein maximally stimulates skeletal muscle protein synthesis in young and elderly subjects. J. Am. Diet. Assoc. 109:1582–86
    [Google Scholar]
  135. 135.
    Tang JE, Moore DR, Kujbida GW, Tarnopolsky MA, Phillips SM 2009. Ingestion of whey hydrolysate, casein, or soy protein isolate: effects on mixed muscle protein synthesis at rest and following resistance exercise in young men. J. Appl. Physiol. 107:987–92
    [Google Scholar]
  136. 136.
    Tarnopolsky MA. 2004. Protein requirements for endurance athletes. Nutrition 20:662–68
    [Google Scholar]
  137. 137.
    Tarnopolsky MA, Atkinson SA, MacDougall JD, Chesley A, Phillips S, Schwarcz HP 1992. Evaluation of protein requirements for trained strength athletes. J. Appl. Physiol. 73:1986–95
    [Google Scholar]
  138. 138.
    Teixeira FJ, Matias CN, Monteiro CP, Valamatos MJ, Reis J et al. 2019. Leucine metabolites do not enhance training-induced performance or muscle thickness. Med. Sci. Sports Exerc. 51:56–64
    [Google Scholar]
  139. 139.
    Thomas DT, Erdman KA, Burke LM 2016. Nutrition and athletic performance. Med. Sci. Sports Exerc. 48:543–68
    [Google Scholar]
  140. 140.
    Tipton KD, Elliott TA, Cree MG, Aarsland AA, Sanford AP, Wolfe RR 2007. Stimulation of net muscle protein synthesis by whey protein ingestion before and after exercise. Am. J. Physiol. Endocrinol. Metab 292:E71–76
    [Google Scholar]
  141. 141.
    Tipton KD, Ferrando AA, Phillips SM, Doyle D Jr, Wolfe RR 1999. Postexercise net protein synthesis in human muscle from orally administered amino acids. Am. J. Physiol. 276:E628–34
    [Google Scholar]
  142. 142.
    Trommelen J, Beelen M, Pinckaers PJ, Senden JM, Cermak NM, van Loon LJ 2016. Fructose coingestion does not accelerate postexercise muscle glycogen repletion. Med. Sci. Sports Exerc. 48:907–12
    [Google Scholar]
  143. 143.
    Tsintzas K, Williams C, Boobis L, Symington S, Moorehouse J et al. 2003. Effect of carbohydrate feeding during recovery from prolonged running on muscle glycogen metabolism during subsequent exercise. Int. J. Sports Med. 24:452–58
    [Google Scholar]
  144. 144.
    Ulbricht A, Gehlert S, Leciejewski B, Schiffer T, Bloch W, Hohfeld J 2015. Induction and adaptation of chaperone-assisted selective autophagy CASA in response to resistance exercise in human skeletal muscle. Autophagy 11:538–46
    [Google Scholar]
  145. 145.
    van Hall G, Shirreffs SM, Calbet JA 2000. Muscle glycogen resynthesis during recovery from cycle exercise: no effect of additional protein ingestion. J. Appl. Physiol. 88:1631–36
    [Google Scholar]
  146. 146.
    van Loon LJ. 2013. Role of dietary protein in post-exercise muscle reconditioning. Nestle. Nutr. Inst. Workshop Ser. 75:73–83
    [Google Scholar]
  147. 147.
    van Loon LJ, Saris WH, Kruijshoop M, Wagenmakers AJ 2000. Maximizing postexercise muscle glycogen synthesis: carbohydrate supplementation and the application of amino acid or protein hydrolysate mixtures. Am. J. Clin. Nutr. 72:106–11
    [Google Scholar]
  148. 148.
    Veech RL. 2004. The therapeutic implications of ketone bodies: the effects of ketone bodies in pathological conditions: ketosis, ketogenic diet, redox states, insulin resistance, and mitochondrial metabolism. Prostaglandins Leukot. Essent. Fatty Acids 70:309–19
    [Google Scholar]
  149. 149.
    Vollestad NK, Tabata I, Medbo JI 1992. Glycogen breakdown in different human muscle fibre types during exhaustive exercise of short duration. Acta Physiol. Scand. 144:135–41
    [Google Scholar]
  150. 150.
    Wallis GA, Hulston CJ, Mann CH, Roper HP, Tipton KD, Jeukendrup AE 2008. Postexercise muscle glycogen synthesis with combined glucose and fructose ingestion. Med. Sci. Sports Exerc. 40:1789–94
    [Google Scholar]
  151. 151.
    Webster CC, Noakes TD, Chacko SK, Swart J, Kohn TA, Smith JA 2016. Gluconeogenesis during endurance exercise in cyclists habituated to a long-term low carbohydrate high-fat diet. J. Physiol. 594:4389–405
    [Google Scholar]
  152. 152.
    West DW, Burd NA, Coffey VG, Baker SK, Burke LM et al. 2011. Rapid aminoacidemia enhances myofibrillar protein synthesis and anabolic intramuscular signaling responses after resistance exercise. Am. J. Clin. Nutr. 94:795–803
    [Google Scholar]
  153. 153.
    Wilkinson SB, Phillips SM, Atherton PJ, Patel R, Yarasheski KE et al. 2008. Differential effects of resistance and endurance exercise in the fed state on signalling molecule phosphorylation and protein synthesis in human muscle. J. Physiol. 586:3701–17
    [Google Scholar]
  154. 154.
    Wilkinson SB, Tarnopolsky MA, Macdonald MJ, Macdonald JR, Armstrong D, Phillips SM 2007. Consumption of fluid skim milk promotes greater muscle protein accretion after resistance exercise than does consumption of an isonitrogenous and isoenergetic soy-protein beverage. Am. J. Clin. Nutr. 85:1031–40
    [Google Scholar]
  155. 155.
    Williams M, Raven PB, Fogt DL, Ivy JL 2003. Effects of recovery beverages on glycogen restoration and endurance exercise performance. J. Strength. Cond. Res. 17:12–19
    [Google Scholar]
  156. 156.
    Willoughby DS, Stout JR, Wilborn CD 2007. Effects of resistance training and protein plus amino acid supplementation on muscle anabolism, mass, and strength. Amino Acids 32:467–77
    [Google Scholar]
  157. 157.
    Witard OC, Jackman SR, Breen L, Smith K, Selby A, Tipton KD 2014. Myofibrillar muscle protein synthesis rates subsequent to a meal in response to increasing doses of whey protein at rest and after resistance exercise. Am. J. Clin. Nutr. 99:86–95
    [Google Scholar]
  158. 158.
    Wojtaszewski JF, MacDonald C, Nielsen JN, Hellsten Y, Hardie DG et al. 2003. Regulation of 5′AMP-activated protein kinase activity and substrate utilization in exercising human skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 284:E813–22
    [Google Scholar]
  159. 159.
    Wojtaszewski JF, Nielsen P, Kiens B, Richter EA 2001. Regulation of glycogen synthase kinase-3 in human skeletal muscle: effects of food intake and bicycle exercise. Diabetes 50:265–69
    [Google Scholar]
  160. 160.
    Yaspelkis BB III, Ivy JL 1999. The effect of a carbohydrate–arginine supplement on postexercise carbohydrate metabolism. Int. J. Sport Nutr. 9:241–50
    [Google Scholar]
  161. 161.
    Yeo WK, Lessard SJ, Chen ZP, Garnham AP, Burke LM et al. 2008. Fat adaptation followed by carbohydrate restoration increases AMPK activity in skeletal muscle from trained humans. J. Appl. Physiol. 105:1519–26
    [Google Scholar]
  162. 162.
    Yeo WK, Paton CD, Garnham AP, Burke LM, Carey AL, Hawley JA 2008. Skeletal muscle adaptation and performance responses to once a day versus twice every second day endurance training regimens. J. Appl. Physiol. 105:1462–70
    [Google Scholar]
  163. 163.
    Zachwieja JJ, Costill DL, Fink WJ 1993. Carbohydrate ingestion during exercise: effects on muscle glycogen resynthesis after exercise. Int. J. Sport Nutr. 3:418–30
    [Google Scholar]
  164. 164.
    Zachwieja JJ, Costill DL, Pascoe DD, Robergs RA, Fink WJ 1991. Influence of muscle glycogen depletion on the rate of resynthesis. Med. Sci. Sports Exerc. 23:44–48
    [Google Scholar]
  165. 165.
    Zawadzki KM, Yaspelkis BB III, Ivy JL 1992. Carbohydrate–protein complex increases the rate of muscle glycogen storage after exercise. J. Appl. Physiol. 72:1854–59
    [Google Scholar]
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