Fuel for the Work Required: A Theoretical Framework for Carbohydrate Periodization and the Glycogen Threshold Hypothesis

Sports Medicine

Volumn 48, Issue 5, 2018, Pages 1031-1048

  Impey, Samuel G ^a   Hearris, Mark A ^a   Hammond, Kelly M ^a   Bartlett, Jonathan D ^b   Louis, Julien ^a   Close, Graeme L ^a   Morton, James P ^a  

^a LIVERPOOL JOHN MOORES UNIVERSITY   (United Kingdom)

^b VICTORIA UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOGEN;

CARBOHYDRATE DIET; ENDURANCE; EXERCISE; HUMAN; METABOLISM; PHYSIOLOGY; SKELETAL MUSCLE; SPORT;

DIETARY CARBOHYDRATES; EXERCISE; GLYCOGEN; HUMANS; MUSCLE, SKELETAL; PHYSICAL ENDURANCE; SPORTS;

EID: 85042064034     PISSN: 01121642     EISSN: 11792035     Source Type: Journal    
DOI: 10.1007/s40279-018-0867-7     Document Type: Article

References (58)

1. Thomas DT, Erdman KA, Burke LM. American college of sports medicine joint position statement. nutrition and athletic performance. Med Sci Sports Exerc. 2016;48:543–68.
2. Bergstrom J, Hermansen L, Hultman E, Saltin B. Diet, muscle glycogen and physical performance. Acta Physiol Scand. 1967;71:140–50.
3. Bergstrom J, Hultman E. Muscle glycogen synthesis after exercise: an enhancing factor localized to the muscle cells in man. Nature. 1966;16:309–10.
4. Bergstrom J, Hultman E. The effect of exercise on muscle glycogen and electrolytes in normals. Scand J Clin Lab Invest. 1966;18:16–20.
5. Hermansen L, Hultman E, Saltin B. Muscle glycogen during prolonged severe exercise. Acta Physiol Scand. 1967;71:129–39.
6. Sherman WM, Costill DL, Fink WJ, Miller JM. Effect of exercise-diet manipulation on muscle glycogen and its subsequent utilization during performance. Int J Sports Med. 1981;2:114–8.
7. Sherman WM, Wimer GS. Insufficient dietary carbohydrate during training? Does it impair athletic performance? Int J Sport Nutr. 1991;1:28–44.
8. Sherman WM, Doyle JA, Lamb DR, Strauss RH. Dietary carbohydrate, muscle glycogen, and exercise performance during 7 days of training. Am J Clin Nutr. 1993;57:27–31.
9. Hansen AK, Fischer CP, Plomgaard P, Andersen JL, Saltin B, Pedersen BK. Skeletal muscle adaptation: training twice every second day vs. training once daily. J Appl Physiol. 2005;98:93–9.
10. Stellingwerff T. Case Study: nutrition and training periodization in three elite marathon runners. Int J Sport Nutri Exerc Metab. 2012;22:392–400.
11. Hawley JA, Morton JP. Ramping up the signal: promoting endurance training adaptation in skeletal muscle by nutritional manipulation. Clin Exp Pharmacol Physiol. 2014;41:608–13.
12. Bartlett JD, Hawley JA, Morton JP. Carbohydrate availability and exercise training adaptation: too much of a good thing? Eur J Sport Sci. 2015;15:3–12.
13. Coyle EF, Coggan AR, Hemmert MK, Ivy JL. Muscle glycogen utilization during strenuous exercise when fed carbohydrate. J Appl Physiol. 1986;61:165–72.
14. Wildrick JJ, Costill DL, Fink WJ, Hickey MS, McConnell GK, Tanaka H. Carbohydrate feedings and exercise performance: effect of initial muscle glycogen concentration. J Appl Physiol. 1993;74:2998–3005.
15. Pilegaard H, Keller C, Steensberg A, Helge JW, Pedersen BK, Saltin B, Neufer PD. Influence of pre-exercise muscle glycogen content on exercise-induced transcriptional regulation of metabolic genes. J Physiol. 2002;541:261–71.
16. Pilegaard H, Osada T, Andersen LT, Helge JW, Saltin B, Neufer PD. Substrate availability and transcriptional regulation of metabolic genes in human skeletal muscle during recovery from exercise. Metabolism. 2005;54:1048–55.
17. Yeo WK, Paton CD, Garnham AP, Burke LM, Carey AL, Hawley JA. Skeletal muscle adaptation and performance responses to once versus twice every second day endurance training regimens. J Appl Physiol. 2008;105:1462–70.
18. Morton JP, Croft L, Bartlett JD, MacLaren DP, Reilly T, Evans L, McArdle A, Drust B. Reduced carbohydrate availability does not modulate training-induced heat shock protein adaptations but does up regulate oxidative enzyme activity in human skeletal muscle. J Appl Physiol. 2009;106:1513–21.
19. Hulston CJ, Venables MC, Mann CH, Martin C, Philp A, Baar K, Jeukendrup AE. Training with low muscle glycogen enhances fat metabolism in well-trained cyclists. Med Sci Sports Exerc. 2010;42:2046–55.
20. Cochran AJ, Myslik F, Maclnnis MJ, Percival ME, Bishop D, Tarnopolsky MA, Gibala MJ. Manipulating carbohydrate availability between twice-daily sessions of high-intensity interval training over 2 weeks improves time-trial performance. Int J Sport Nutr Exerc Metab. 2015;25:463–70.
21. Steinberg GR, Watt MJ, McGee SL, Chan S, Hargreaves M, Febbraio MA, Stapleton D, Kemp BE. Reduced glycogen availability is associated with increased AMPKalpha2 activity, nuclear AMPKalpha2 protein abundance, and GLUT4 mRNA expression in contracting human skeletal muscle. Appl Physiol Nutr Metab. 2006;31:302–12.
22. Cochran AJ, Little JP, Tarnopolsky MA, Gibala MJ. Carbohydrate feeding during recovery alters the skeletal muscle metabolic response to repeated sessions of high-intensity interval exercise in humans. J Appl Physiol. 2010;108:628–36.
23. Yeo WK, McGee SL, Carey AL, Paton CD, Garnham AP, Hargreaves M, Hawley JA. Acute signalling responses to intense endurance training commenced with low or normal muscle glycogen. Exp Physiol. 2010;95:351–8.
24. Psilander N, Frank P, Flockhart M, Sahlin K. Exercise with low glycogen increases PGC-1a gene expression in human skeletal muscle. Eur J Appl Physiol. 2013;113:951–63.
25. Horowitz JF, Mora-Rodriguez R, Byerley LO, Coyle EF. Lipolytic suppression following carbohydrate ingestion limits fat oxidation during exercise. Am J Physiol. 1997;273:768–75.
26. Arkinstall MJ, Bruce CR, Nikolopoulos V, Garnham AP, Hawley JA. Effect of carbohydrate ingestion on metabolism during running and cycling. J Appl Physiol. 2001;91:2125–34.
27. Akerstrom TCA, Birk JB, Klein DK, Erikstrup C, Plomgaard P, Pedersen BK, Wojtaszewski J. Oral glucose ingestion attenuates exercise-induced activation of 5′-AMP-activated protein kinase in human skeletal muscle. Biochem Biophys Res Commun. 2006;342:949–55.
28. Civitarese AE, Hesselink MK, Russell AP, Ravussin E, Schrauwen P. Glucose ingestion during exercise blunts exercise-induced gene expression of skeletal muscle fat oxidative genes. Am J Physiol Endocrinol Metab. 2005;289:1023–9.
29. Cluberton LJ, McGee SL, Murphy RM, Hargreaves M. Effect of carbohydrate ingestion on exercise-induced alterations in metabolic gene expression. J Appl Physiol. 2005;99:1359–63.
30. Van Proeyen K, Szlufcik K, Nielens H, Ramaekers M, Hespel P. Beneficial metabolic adaptations due to endurance exercise training in the fasted state. J Appl Physiol. 2011;110:236–45.
31. De Bock K, Derave W, Eijnde BO, Hesselink MK, Koninckx E, Rose AJ, Schrauwen P, Bonen A, Richter EA, Hespel P. Effect of training in the fasted state on metabolic responses during exercise with carbohydrate intake. J Appl Phyiol. 2008;104:1045–55.
32. Nybo L, Pedersen K, Christensen B, Aagaard P, Brandt N, Kiens B. Impact of carbohydrate supplementation during endurance training on glycogen storage and performance. Acta Physiol. 2009;197:117–27.
33. Impey SG, Smith D, Robinson AL, Owens DJ, Bartlett JD, Smith K, Limb M, Tang J, Fraser WD, Close GL, Morton JP. Leucine-enriched protein feeding does not impair exercise-induced free fatty acid availability and lipid oxidation: beneficial implications for training in carbohydrate-restricted states. Amino Acids. 2015;47:407–16.
34. Taylor C, Bartlett JD, van de Graaf CS, Louhelainen J, Coyne V, Iqbal Z, MacLaren DP, Gregson W, Close GL, Morton JP. Protein ingestion does not impair exercise-induced AMPK signalling when in a glycogen-depleted state: implications for train-low compete-high. Eur J Appl Physiol. 2013;113:1457–68.
35. Hulston CJ, Wolsk E, Grøndahl TS, Yfanti C, Van Hall G. Protein intake does not increase vastus lateralis muscle protein synthesis during cycling. Med Sci Sports Exerc. 2011;43:1635–42.
36. Wojtaszewski JF, MacDonald C, Nielsen JN, Hellsten Y, Hardie DG, Kemp BE, Kiens B, Richter EA. Regulation of 5′AMP-activated protein kinase activity and substrate utilization in exercising human skeletal muscle. Am J Physiol Endocrinol Metab. 2003;284:E812–22.
37. Chan S, McGee SL, Watt MJ, Hargreaves M, Febbraio MA. Altering dietary nutrient intake that reduces glycogen content leads to phosphorylation of nuclear p38 MAP kinase in human skeletal muscle: association with IL-6 gene transcription during contraction. FASEB J. 2004;18:1785–7.
38. Bartlett JD, Louhelainen J, Iqbal Z, Cochran AJ, Gibala MJ, Gregson W, Close GL, Drust B, Morton JP. Reduced carbohydrate availability enhances exercise-induced p53 signalling in human skeletal muscle: implications for mitochondrial biogenesis. Am J Physiol Regul Integr Comp Physiol. 2013;304:450–8.
39. Lane SC, Camera DM, Lassiter DG, Areta JL, Bird SR, Yeo WK, Jeacocke NA, Krook A, Zierath JR, Burke LM, Hawley JA. Effects of sleeping with reduced carbohydrate availability on acute training responses. J Appl Physiol. 2015;119:643–55.
40. Marquet LA, Brisswalter J, Louis J, Tiollier E, Burke LM, Hawley JA, Hausswirth C. Enhanced endurance performance by periodization of carbohydrate intake: “Sleep low” strategy. Med Sci Sports Exerc. 2016;48:663–72.
41. Marquet LA, Hausswirth C, Molle O, Hawley JA, Burke LM, Tiollier E, Brisswalter J. Periodization of carbohydrate intake: short-term effect on performance. Nutrients. 2016;8:755.
42. Zbinden-Foncea H, van Loon LJ, Raymackers JM, Francaux M, Deldicque L. Contribution of nonesterified fatty acids to mitogen-activated protein kinase activation in human skeletal muscle during endurance exercise. Int J Sport Nutr Exerc Metab. 2013;23:201–9.
43. Hammond KM, Impey SG, Currell K, Mitchell N, Shepherd SO, Jeromson S, Hawley JA, Close GL, Hamilton LD, Sharples AP, Morton JP. Postexercise high-fat feeding suppresses p70S6K1 activity in human skeletal muscle. Med Sci Sport Exerc. 2016;48:2108–17.
44. Stellingwerff T, Spriet LL, Watt MJ, Kimber NE, Hargreaves M, Hawley JA, Burke LM. Decreased PDH activation and glycogenolysis during exercise following fat adaptation with carbohydrate restoration. Am J Physiol Endocrinol Metab. 2006;290:380–8.
45. Burke LM, Ross ML, Garvican-Lewis LA, Welvaert M, Heikura IA, Forbes SG, Mirtschin JG, Cato LE, Strobel N, Sharma AP, Hawley JA. Low carbohydrate, high fat diet impairs exercise economy and negates the performance benefit from intensified training in elite race walkers. J Physiol. 2017;595:2785–807.
46. Stephens FB, Chee C, Wall BT, Murton AJ, Shannon CE, van Loon LJ, Tsintzas K. Lipid-induced insulin resistance is associated with an impaired skeletal muscle protein synthetic response to amino acid ingestion in healthy young men. Diabetes. 2015;64:1615–20.
47. Vogt S, Heinrich L, Schumacher YO, Grosshauser M, Blum A, König D, Berg A, Schmid A. Energy intake and energy expenditure of elite cyclists during preseason training. Int J Sports Med. 2005;26:701–6.
48. Impey SG, Hammond KM, Shepherd SO, Sharples AP, Stewart C, Limb M, Smith K, Philp A, Jeromson S, Hamilton DL, Close GL, Morton JP. Fuel for the work required: a practical approach to amalgamating train-low paradigms for endurance athletes. Physiol Rep. 2016;4:e12803.
49. Lee-Young RS, Palmer MJ, Linden KC, LePlastrier K, Canny BJ, Hargreaves M, Wadley GD, Kemp BE, McConell GK. Carbohydrate ingestion does not alter skeletal muscle AMPK signalling during exercise in humans. Am J Physiol Endocrinol Metab. 2006;291:566–73.
50. 2+ kinetics in human skeletal muscle. J Physiol. 2011;589:711–25.
51. Duhamel TA, Perco JG, Green HJ. Manipulation of dietary carbohydrates after prolonged effort modifies muscle sarcoplasmic reticulum responses in exercising males. Am J Physiol Regul Integr Comp Physiol. 2006;291:1100–10.
52. 2+ release rate in elite endurance athletes. Med Sci Sports Exerc. 2014;46:496–505.
53. Costa RJ, Jones GE, Lamb KL, Coleman R, Williams JH. The effects of a high carbohydrate diet on cortisol and salivary immunoglobulin A (s-IgA) during a period of increase exercise workload amongst Olympic and Ironman triathletes. Int J Sports Med. 2005;26:880–6.
54. Jensen L, Gejl KD, Ørtenblad N, Nielsen JL, Bech RD, Nygaard T, Sahlin K, Frandsen U. Carbohydrate restricted recovery from long term endurance exercise does not affect gene responses involved in mitochondrial biogenesis in highly trained athletes. Physiol Rep. 2015;12:e121814.
55. Gejl KD, Thams L, Hansen M, Rokkedal-Lausch T, Plomgaard P, Nybo L, Larsen FJ, Cardinale DA, Jensen K, Holmberg HC, Vissing K, Ørtenblad N. No superior adaptations to carbohydrate periodization in elite endurance athletes. Med Sci Sports Exerc. 2017;49(12):2486–97.
56. Lane SC, Areta JL, Bird SR, Coffey VG, Burke LM, Desbrow B, Karagounis LG, Hawley JA. Caffeine ingestion and cycling power output in a low or normal muscle glycogen state. Med Sci Sports Exerc. 2013;45:1577–84.
57. Gollnick PD, Piehl K, Saltin B. Selective glycogen depletion pattern in human skeletal muscle fibres after exercise of varying intensity and at varying pedalling rates. J Physiol. 1974;241:45–57.
58. De Bock K, Derave W, Ramaekers M, Richter EA, Hespel P. Fiber type-specific muscle glycogen sparing due to carbohydrate intake before and during exercise. J Appl Physiol. 2007;102 (1):183–8.