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Sports Medicine

, Volume 43, Issue 11, pp 1139–1155 | Cite as

The Use of Carbohydrates During Exercise as an Ergogenic Aid

  • Naomi M. Cermak
  • Luc J. C. van Loon
Review Article

Abstract

Carbohydrate and fat are the two primary fuel sources oxidized by skeletal muscle tissue during prolonged (endurance-type) exercise. The relative contribution of these fuel sources largely depends on the exercise intensity and duration, with a greater contribution from carbohydrate as exercise intensity is increased. Consequently, endurance performance and endurance capacity are largely dictated by endogenous carbohydrate availability. As such, improving carbohydrate availability during prolonged exercise through carbohydrate ingestion has dominated the field of sports nutrition research. As a result, it has been well-established that carbohydrate ingestion during prolonged (>2 h) moderate-to-high intensity exercise can significantly improve endurance performance. Although the precise mechanism(s) responsible for the ergogenic effects are still unclear, they are likely related to the sparing of skeletal muscle glycogen, prevention of liver glycogen depletion and subsequent development of hypoglycemia, and/or allowing high rates of carbohydrate oxidation. Currently, for prolonged exercise lasting 2–3 h, athletes are advised to ingest carbohydrates at a rate of 60 g·h−1 (~1.0–1.1 g·min−1) to allow for maximal exogenous glucose oxidation rates. However, well-trained endurance athletes competing longer than 2.5 h can metabolize carbohydrate up to 90 g·h−1 (~1.5–1.8 g·min−1) provided that multiple transportable carbohydrates are ingested (e.g. 1.2 g·min−1 glucose plus 0.6 g·min−1 of fructose). Surprisingly, small amounts of carbohydrate ingestion during exercise may also enhance the performance of shorter (45–60 min), more intense (>75 % peak oxygen uptake; VO2peak) exercise bouts, despite the fact that endogenous carbohydrate stores are unlikely to be limiting. The mechanism(s) responsible for such ergogenic properties of carbohydrate ingestion during short, more intense exercise bouts has been suggested to reside in the central nervous system. Carbohydrate ingestion during exercise also benefits athletes involved in intermittent/team sports. These athletes are advised to follow similar carbohydrate feeding strategies as the endurance athletes, but need to modify exogenous carbohydrate intake based upon the intensity and duration of the game and the available endogenous carbohydrate stores. Ample carbohydrate intake is also important for those athletes who need to compete twice within 24 h, when rapid repletion of endogenous glycogen stores is required to prevent a decline in performance. To support rapid post-exercise glycogen repletion, large amounts of exogenous carbohydrate (1.2 g·kg−1·h−1) should be provided during the acute recovery phase from exhaustive exercise. For those athletes with a lower gastrointestinal threshold for carbohydrate ingestion immediately post-exercise, and/or to support muscle re-conditioning, co-ingesting a small amount of protein (0.2–0.4 g·kg−1·h−1) with less carbohydrate (0.8 g·kg−1·h−1) may provide a feasible option to achieve similar muscle glycogen repletion rates.

Keywords

Muscle Glycogen Carbohydrate Ingestion Prolonged Exercise Carbohydrate Solution Carbohydrate Feeding 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

No sources of funding were used to prepare this manuscript. The authors have no conflicts of interest to declare that are directly relevant to the content of this review.

References

  1. 1.
    Romijn J, Coyle E, Sidossis L, et al. Regulation of endogenous fat and carbohydrate metabolism in relation to exercise intensity and duration. Am J Physiol. 1993;265:E380–91.PubMedGoogle Scholar
  2. 2.
    van Loon L, Greenhaff P, Constantin-Teodosiu D, et al. The effects of increasing exercise intensity on muscle fuel utilisation in humans. J Physiol. 2001;536:295–304.PubMedGoogle Scholar
  3. 3.
    van Loon L, Jeukendrup A, Saris W, et al. Effect of training status on fuel selection during submaximal exercise with glucose ingestion. J Appl Physiol. 1999;87(4):1413–20.PubMedGoogle Scholar
  4. 4.
    McArdle W, Katch F, Katch V. Carbohydrates, lipids, and proteins. In: Darcy P, editor. Exercise physiology. Baltimore Lippincott Williams & Wilkins; 2001. p. 11–3.Google Scholar
  5. 5.
    Tsintzas K, Williams C. Human muscle glycogen metabolism during exercise. Effect of carbohydrate supplementation. Sports Med. 1998;25(1):7–23.PubMedGoogle Scholar
  6. 6.
    Bergstrom J, Hultman E. A study of the glycogen metabolism during exercise in man. Scand J Clin Lab Invest. 1967;19:218–28.PubMedGoogle Scholar
  7. 7.
    Jeukendrup A. Carbohydrate intake during exercise and performance. Nutrition. 2004;20:669–77.PubMedGoogle Scholar
  8. 8.
    Krogh A, Lindhard J. The relative value of fat and carbohydrate as sources of muscular energy. Biochem J. 1920;14(3–4):290–363.PubMedGoogle Scholar
  9. 9.
    Levine S, Gordon B, Derick C. Some changes in chemical constituents of blood following a marathon race. JAMA. 1924;82:1778.Google Scholar
  10. 10.
    Gordon B, Kohn L, Levine S, et al. Sugar content of the blood in runners following a marathon race with especial reference to the prevention of hypoglyemia: further observations. JAMA. 1925;85(7):508–9.Google Scholar
  11. 11.
    Christensen E. Der Stoffwechsel und die Respiratorischen Funktionen bei schwerer korperlicher Arbeit. Scand Arch Physiol. 1932;81:160–71.Google Scholar
  12. 12.
    Bergstrom J, Hultman E. Muscle glycogen synthesis after exercise: an enhancing factor localized in muscle cells in man. Nature. 1966;210(5033):309–10.PubMedGoogle Scholar
  13. 13.
    Bergstrom J, Hermansen L, Hultman E, et al. Diet, muscle glycogen and physical performance. Acta Physiol Scand. 1967;71:140–50.PubMedGoogle Scholar
  14. 14.
    Hawley J, Schabort E, Noakes T, et al. Carbohydrate-loading and exercise performance. An update. Sports Med. 1997;24(2):73–81.PubMedGoogle Scholar
  15. 15.
    Bonen A, Malcolm S, Kilgour R, et al. Glucose ingestion before and during intense exercise. J Appl Physiol. 1981;50(4):766–71.PubMedGoogle Scholar
  16. 16.
    Felig P, Cherif A, Minagawa A, et al. Hypolgycemia during prolonged exercise in normal men. N Engl J Med. 1982;306(15):395–900.Google Scholar
  17. 17.
    Ivy J, Costill D, Fink W, et al. Influence of caffeine and carbohydrate feedings on endurance performance. Med Sci Sports Exerc. 1979;11(1):6–11.Google Scholar
  18. 18.
    Coyle E, Coggan A, Hemert M, et al. Muscle glycogen utilization during prolonged strenuous exercise when fed carbohydrate. J Appl Physiol. 1986;61(1):165–72.PubMedGoogle Scholar
  19. 19.
    Coyle E, Hagberg J, Hurley B, et al. Carbohydrate feeding during prolonged strenuous exercise can delay fatigue. J Appl Physiol. 1983;55:230–5.PubMedGoogle Scholar
  20. 20.
    Fielding R, Costill D, Fink W, et al. Effect of carbohydrate feeding frequencies and dosage on muscle glycogen use during exercise. Med Sci Sports Exerc. 1985;17(4):472–6.PubMedGoogle Scholar
  21. 21.
    Hargreaves M, Costill D, Coggan A, et al. Effect of carbohydrate feedings on muscle glycogen utilization and exercise performance. Med Sci Sports Exerc. 1984;16(3):219–22.PubMedGoogle Scholar
  22. 22.
    Ivy J, Miller W, Dover V, et al. Endurance improved by ingestion of a glucose polymer supplement. Med Sci Sports Exerc. 1983;15(6):466–71.PubMedGoogle Scholar
  23. 23.
    Mitchell J, Costill D, Houmard J, et al. Effects of carbohydrate ingestion on gastric emptying and exercise performance. Med Sci Sports Exerc. 1988;20(2):110–5.PubMedGoogle Scholar
  24. 24.
    Neufer P, Costill D, Flynn M, et al. Improvements in exercise performance: effects of carbohydrate feedings and diet. J Appl Physiol. 1987;62(3):983–8.PubMedGoogle Scholar
  25. 25.
    Bjorkman O, Sahlin K, Hagenfeldt L, et al. Influence of glucose and fructose ingestion on the capacity for long-term exercise in well-trained men. Clin Physiol. 1984;4:483–94.PubMedGoogle Scholar
  26. 26.
    Coggan A, Coyle E. Reversal of fatigue during prolonged exercise by carbohydrate infusion or ingestion. J Appl Physiol. 1987;63(6):2388–95.PubMedGoogle Scholar
  27. 27.
    Angus D, Hargreaves M, Dancey J, et al. Effect of carbohydrate or carbohydrate plus medium-chain triglyceride ingestion on cycling time trial performance. J Appl Physiol. 2000;88(1):113–9.PubMedGoogle Scholar
  28. 28.
    Tsintzas O, Williams C, Boobis L, et al. Carbohydrate ingestion and single muscle fiber glycogen metabolism during prolonged running in men. J Appl Physiol. 1996;81(2):801–9.PubMedGoogle Scholar
  29. 29.
    Maughan R, Bethell L, Leiper J. Effects of ingested fluids on exercise capacity and on cardiovascular and metabolic responses to prolonged exercise in man. Exp Physiol. 1996;81(5):847–59.PubMedGoogle Scholar
  30. 30.
    Langenfeld M, Seifert J, Rudge S, et al. Effect of carbohydrate ingestion on performance of non-fasted cyclists during a simulated 80-mile time trial. J Sports Med Phys Fitness. 1994;34(3):263–70.PubMedGoogle Scholar
  31. 31.
    Tsintzas K, Liu R, Williams C, et al. The effect of carbohydrate ingestion on performance during a 30-km race. Int J Sport Nutr. 1993;3(2):127–39.PubMedGoogle Scholar
  32. 32.
    Wright D, Sherman W, Dernbach A. Carbohydrate feedings before, during, or in combination improve cycling endurance performance. J Appl Physiol. 1991;71(3):1082–8.PubMedGoogle Scholar
  33. 33.
    Murray R, Eddy D, Murray T, et al. The effect of fluid and carbohydrate feedings during intermittent cycling exercise. Med Sci Sports Exerc. 1987;19(6):597–604.PubMedGoogle Scholar
  34. 34.
    Vandenbogaerde T, Hopkins W. Effects of acute carbohydrate supplementation on endurance performance. Sports Med. 2011;41(9):773–92.PubMedGoogle Scholar
  35. 35.
    Hulston C, Jeukendrup A. No placebo effect from carbohydrate intake during prolonged exercise. Int J Sport Nutr Exerc Metab. 2009;19(3):275–84.PubMedGoogle Scholar
  36. 36.
    Tsintzas O, Williams C, Boobis L, et al. Carbohydrate ingestion and glycogen utilization in different muscle fibre types in man. J Physiol. 1995;489(Pt 1):243–50.PubMedGoogle Scholar
  37. 37.
    Tsintzas O, Williams C, Constantin-Teodosiu D, et al. Phosphocreatine degradation in type I and type II muscle fibres during submaximal exercise in man: effect of carbohydrate ingestion. J Physiol. 2001;15(537):305–11.Google Scholar
  38. 38.
    Stellingwerff T, Boon H, Gijsen AP, et al. Carbohydrate supplementation during prolonged cycling exercise spares muscle glycogen but does not affect intramyocellular lipid use. Pflugers Arch. 2007;454(4):635–47.PubMedGoogle Scholar
  39. 39.
    Erickson M, Schwartzkopf R, McKenzie R. Effects of caffeine, fructose and glucose ingestion on muscle glycogen utilization during exercise. Med Sci Sports Exerc. 1987;19:579–83.PubMedGoogle Scholar
  40. 40.
    Flynn M, Costill D, Hawley J, et al. Influence of selected carbohydrate drinks on cycling performance and glycogen use. Med Sci Sports Exerc. 1987;19(1):37–40.PubMedGoogle Scholar
  41. 41.
    Mitchell J, Costill D, Houmard J, et al. Influence of carbohydrate dosage on exercise performance and glycogen metabolism. J Appl Physiol. 1989;67(5):1843–9.PubMedGoogle Scholar
  42. 42.
    Hargreaves M, Briggs C. Effect of carbohydrate ingestion on exercise metabolism. J Appl Physiol. 1988;65(4):1553–5.PubMedGoogle Scholar
  43. 43.
    Gollnick P, Piehl K, Saltin B. Selective glycogen depletion pattern in human muscle fibres after exercise of varying intensity and at varying pedalling rates. J Physiol. 1974;241:45–57.PubMedGoogle Scholar
  44. 44.
    Nybo L. CNS fatigue and prolonged exercise: effect of glucose supplementation. Med Sci Sports Exerc. 2003;35(4):589–94.PubMedGoogle Scholar
  45. 45.
    Bosch A, Dennis S, Noakes T. Influence of carbohydrate ingestion on fuel substrate turnover and oxidation during prolonged exercise. J Appl Physiol. 1994;76:2364–72.PubMedGoogle Scholar
  46. 46.
    Jeukendrup A, Raben A, Gijsen A, et al. Glucose kinetics during prolonged exercise in highly trained human subjects: effect of glucose ingestion. J Physiol. 1999;515(Prt 2):579–89.Google Scholar
  47. 47.
    Howlett K, Angus D, Proietto J, et al. Effect of increased blood glucose availability on glucose kinetics during exercise. J Appl Physiol. 1998;84(4):1413–7.PubMedGoogle Scholar
  48. 48.
    Claassen A, Lambert E, Bosch A, et al. Variability in exercise capacity and metabolic response during endurance exercise after a low carbohydrate diet. Int J Sport Nutr Exerc Metab. 2005;15(2):97–116.PubMedGoogle Scholar
  49. 49.
    Jeukendrup A. Carbohydrate and exercise performance: the role of multiple transportable carbohydrates. Curr Opin Clin Nutr Metab Care. 2010;13:452–7.PubMedGoogle Scholar
  50. 50.
    Jeukendrup A, Jentjiens R. Oxidation of carbohydrate feedings during prolonged exercise: current thoughts, guidelines and directions for future research. Sports Med. 2000;29:407–24.PubMedGoogle Scholar
  51. 51.
    Burelle Y, Lamoureux M, Peronnet F, et al. Comparison of exogenous glucose, fructose and galactose oxidation during exercise using 13C-labeling. Br J Nutr. 2006;96(1):56–61.PubMedGoogle Scholar
  52. 52.
    Leijssen D, Saris W, Jeukendrup A, et al. Oxidation of exogenous [13C]glucose during exercise. J Appl Physiol. 1995;79(3):720–5.PubMedGoogle Scholar
  53. 53.
    Rowlands D, Wallis G, Shaw C, et al. Glucose polymer molecular weight does not affect exogenous carbohydrate oxidation. Med Sci Sports Exerc. 2005;37(9):1510–6.PubMedGoogle Scholar
  54. 54.
    Sawka M, Burke L, Eichnet E, et al. American College of Sports Medicine position stand: exercise and fluid replacement. Med Sci Sports Exerc. 2007;39(2):377–90.PubMedGoogle Scholar
  55. 55.
    Rodriguez N, Di Marco N, Langley S. American College of Sports Medicine position stand: nutrition and athletic performance. Med Sci Sports Exerc. 2009;41(3):709–31.PubMedGoogle Scholar
  56. 56.
    Pfeiffer B, Stellingwerff T, Hodgson A, et al. Nutritional intake and gastrointestinal problems during competitive endurance events. Med Sci Sports Exerc. 2012;44(2):344–51.PubMedGoogle Scholar
  57. 57.
    Smith J, Pascoe D, Passe D, et al. Curvilinear dose-response relationship of carbohydrate (0–120 g·h−1) and performance. Med Sci Sports Exerc. 2013;45(2):336–41.PubMedGoogle Scholar
  58. 58.
    Smith J, Zachwieja J, Peronnet F, et al. Fuel selection and cycling endurance performance with ingestion of [13C]glucose: evidence for a carbohydrate dose response. J Appl Physiol. 2010;108(6):1520–9.PubMedGoogle Scholar
  59. 59.
    Hulston C, Wallis G, Jeukendrup A. Exogenous CHO oxidation with glucose plus fructose intake during exercise. Med Sci Sports Exerc. 2009;41:357–63.PubMedGoogle Scholar
  60. 60.
    Jentjens R, Achten J, Jeukendrup A. High oxidation rates from combined carbohydrates ingested during exercise. Med Sci Sports Exerc. 2004;36:1551–8.PubMedGoogle Scholar
  61. 61.
    Jentjens R, Jeukendrup A. High rates of exogenous carbohydrate oxidation from a mixture of glucose and fructose ingested during prolonged cycling exercise. Br J Nutr. 2005;93(4):485–92.PubMedGoogle Scholar
  62. 62.
    Jentjens R, Moseley L, Waring R, et al. Oxidation of combined ingestion of glucose and fructose during exercise. J Appl Physiol. 2004;96(4):1277–84.PubMedGoogle Scholar
  63. 63.
    Jentjens R, Shaw C, Birtles T, et al. Oxidation of combined ingestion of glucose and sucrose during exercise. Metabolism. 2005;54(5):610–8.PubMedGoogle Scholar
  64. 64.
    Jentjens R, Underwood K, Achten J, et al. Exogenous carbohydrate oxidation rates are elevated after combined ingestion of glucose and fructose during exercise in the heat. J Appl Physiol. 2006;100(3):807–16.PubMedGoogle Scholar
  65. 65.
    Jentjens R, Venables M, Jeukendrup A. Oxidation of exogenous glucose, sucrose and maltose during prolonged cycling execise. J Appl Physiol. 2004;96:1285–91.PubMedGoogle Scholar
  66. 66.
    Jeukendrup A, Moseley L, Mainwaring G, et al. Exogenous carbohydrate oxidation during ultra endurance exercise. J Appl Physiol. 2006;100(4):1134–41.PubMedGoogle Scholar
  67. 67.
    Rowlands DS, Thorburn MS, Thorp RM, et al. Effect of graded fructose coingestion with maltodextrin on exogenous 14C-fructose and 13C-glucose oxidation efficiency and high-intensity cycling performance. J Appl Physiol. 2008;104(6):1709–19.PubMedGoogle Scholar
  68. 68.
    Currell K, Jeukendrup A. Superior endurance performance with ingestion of multiple transportable carbohydrates. Med Sci Sports Exerc. 2008;40:275–81.PubMedGoogle Scholar
  69. 69.
    Jeukendrup A. Carbohydrate feeding during exercise. Eur J Sport Sci. 2008;8:77–86.Google Scholar
  70. 70.
    Kellett G. The facilitated component of intestinal glucose absorption. J Physiol. 2001;531:585–95.PubMedGoogle Scholar
  71. 71.
    Ferraris R, Diamond J. Regulation of intestinal sugar transport. Physiol Rev. 1997;77(1):257–302.PubMedGoogle Scholar
  72. 72.
    Janssen G, Kuipers H, Willems G, et al. Plasma activity of muscle enzymes: quantification of skeletal muscle damage and relationship with metabolic variables. Int J Sports Med. 1989;10(Suppl 3):S160–8.PubMedGoogle Scholar
  73. 73.
    Wallis G, Rowlands D, Shaw C, et al. Oxidation of combined ingestion of maltodextrins and fructose during exercise. Med Sci Sports Exerc. 2005;37(3):426–32.PubMedGoogle Scholar
  74. 74.
    Rowlands D, Swift M, Ros M, et al. Composite versus single transportable carbohydrate solution enhances race and laboratory cycling performance. Appl Physiol Nutr Metab. 2012;37(3):425–36.PubMedGoogle Scholar
  75. 75.
    O’Brien W, Rowlands D. Fructose-maltodextrin ratio in a carbohydrate-electrolyte solution differentially affects exogenous carbohydrate oxidation rate, gut comfort, and performance. Am J Physiol Gastrointest Liver Physiol. 2011;300(1):G181–9.PubMedGoogle Scholar
  76. 76.
    Cox G, Clark S, Cox A, et al. Daily training with high carbohydrate availability increases exogenous carbohydrate oxidation during endurance cycling. J Appl Physiol. 2010;109(1):126–34.PubMedGoogle Scholar
  77. 77.
    Pfeiffer B, Stellingwerff T, Zaltas E, et al. Oxidation of solid versus liquid carbohydrate sources during exercise. Med Sci Sports Exerc. 2010;42(11):2030–7.PubMedGoogle Scholar
  78. 78.
    Pfeiffer B, Stellingwerff T, Zaltas E, et al. Carbohydrate oxidation from a carbohydrate gel compared to a drink during exercise. Med Sci Sports Exerc. 2010;42(11):2038–45.PubMedGoogle Scholar
  79. 79.
    Murdoch S, Bazzarre T, Snider I, et al. Differences in the effects of carbohydrate food form on endurance performance to exhaustion. Int J Sport Nutr. 1993;3(1):41–54.PubMedGoogle Scholar
  80. 80.
    Lugo M, Sherman W, Wimer G, et al. Metabolic responses when different forms of carbohydrate energy are consumed during cycling. Int J Sport Nutr. 1993;3(4):398–407.PubMedGoogle Scholar
  81. 81.
    Neufer P, Costill D, Fink W, et al. Effects of exercise and carbohydrate composition on gastric emptying. Med Sci Sports Exerc. 1986;18(6):658–62.PubMedGoogle Scholar
  82. 82.
    Carter J, Jeukendrup A, Mundel T, et al. Carbohydrate supplementation improves moderate and high-intensity exercise in the heat. Pflugers Arch. 2003;446(2):211–9.PubMedGoogle Scholar
  83. 83.
    Jeukendrup A, Brouns F, Wagenmakers A, et al. Carbohydrate-electrolyte feedings improve 1 h time trial cycling performance. Int J Sports Med. 1997;18(2):25–9.Google Scholar
  84. 84.
    Below P, Mora-Rodríguez R, González-Alonso J, et al. Fluid and carbohydrate ingestion independently improve performance during 1 h of intense exercise. Med Sci Sports Exerc. 1995;27(2):200–10.PubMedGoogle Scholar
  85. 85.
    el-Sayed M, Balmer J, Rattu A. Carbohydrate ingestion improves endurance performance during a 1 h simulated time trial. J Sports Sci. 1997;15(2):223–30.Google Scholar
  86. 86.
    Anantaraman R, Carmines A, Gaesser G, et al. Effects of carbohydrate supplementation on performance during 1 h of high intensity exercise. Int J Sports Med. 1995;16(7):461–5.PubMedGoogle Scholar
  87. 87.
    Carter J, Jeukendrup A, Mann C, et al. The effect of glucose infusion on glucose kinetics during a 1-h time trial. Med Sci Sports Exerc. 2004;36(9):1543–50.PubMedGoogle Scholar
  88. 88.
    Carter J, Jeukendrup A, Mann C, et al. The effect of carbohydrate mouth rinse on 1-h cycle time trial performance. Med Sci Sports Exerc. 2004;36(9):1543–50.PubMedGoogle Scholar
  89. 89.
    Gant N, Stinear C, Byblow W. Carbohydrate in the mouth immediately facilitates motor output. Brain Res. 2010;1350:151–8.PubMedGoogle Scholar
  90. 90.
    Maresch C, Herrera-Soto J, Armstrong L, et al. Perceptual responses in the heat after brief intravenous versus oral rehydration. Med Sci Sports Exerc. 2001;33(6):1039–45.Google Scholar
  91. 91.
    Riebe D, Maresch C, Armstrong L. Effects of oral and intravenous rehydration on ratings of perceived exertion and thirst. Med Sci Sports Exerc. 1997;29(1):117–24.PubMedGoogle Scholar
  92. 92.
    Beelen M, Berghuis J, Bonaparte B, et al. Carbohydrate mouth rinsing in the fed state: lack of enhancement of time-trial performance. Int J Sport Nutr Exerc Metab. 2009;19:400–9.PubMedGoogle Scholar
  93. 93.
    Chambers E, Bridge M, Jones D. Carbohydrate sensing in the human mouth: effects on exercise performance and brain activity. J Physiol. 2009;578(8):1779–94.Google Scholar
  94. 94.
    Fares E, Kayser B. Carbohydrate mouth rinse effects on exercise capacity in pre and postprandial states. J Nutr Metab. 2011;385962.Google Scholar
  95. 95.
    Pottier A, Bouckaert J, Gilis W, et al. Mouth rinse but not ingestion of a carbohydrate solution improves 1-h cycle time trial performance. Scand J Med Sci Sports. 2010;20(1):105–11.PubMedGoogle Scholar
  96. 96.
    Rollo I, Cole M, Miller R, et al. The influence of mouth-rinsing a carbohydrate solution on 1 hour running performance. Med Sci Sports Exerc. 2010;42(4):798–804.PubMedGoogle Scholar
  97. 97.
    Whitham M, McKinney J. Effect of a carbohydrate mouthwash on running time-trial performance. J Sports Sci. 2007;25(12):1385–92.PubMedGoogle Scholar
  98. 98.
    Rollo I, Williams C, Nevill M. Influence of ingesting versus mouth rinsing a carbohydrate solution during a 1-h run. Med Sci Sports Exerc. 2011;43(3):468–75.PubMedGoogle Scholar
  99. 99.
    Haase L, Cerf-Ducastel B, Murphy C. Cortical activation in response to pure taste stimuli during the physiological states of hunger and satiety. Neuroimage. 2009;44(3):1008–21.PubMedGoogle Scholar
  100. 100.
    Frank G, Oberndorfer T, Simmons A, et al. Sucrose activates human taste pathways differently from artificial sweetener. Neuroimage. 2008;39(4):1559–69.PubMedGoogle Scholar
  101. 101.
    Lane S, Bird S, Burke L, et al. Effect of a carbohydrate mouth rinse on simulated cycling time-trial performance commenced in a fed or fasted state. Appl Physiol Nutr Metab. 2013;28(2):134–9.Google Scholar
  102. 102.
    Gam S, Guelfi K, Fournier P. Opposition of carbohydrate in a mouth-rinse solution to the detrimental effect of mouth rinsing during cycling time trials. Int J Sport Nutr Exerc Metab. 2013;23(1):48–56.Google Scholar
  103. 103.
    Clark V, Hopkins W, Hawley J, et al. Placebo effect of carbohydrate feedings during a 40-km cycling time trial. Med Sci Sports Exerc. 2000;32(9):1642–7.PubMedGoogle Scholar
  104. 104.
    Rollo I, Williams C. Effect of mouth-rinsing carbohydrate solutions on endurance performance. Sports Med. 2011;41(6):449–61.PubMedGoogle Scholar
  105. 105.
    Jeukendrup A, Chambers E. Oral carbohydrate sensing and exercise performance. Curr Opin Clin Nutr Metab Care. 2010;13(4):447–51.PubMedGoogle Scholar
  106. 106.
    Bangsbo J. The physiology of soccer with special reference to intense intermittent exercise. Acta Physiol Scand. 1994;619(Suppl):1–155.Google Scholar
  107. 107.
    Balsom P, Wood K, Olsson P, et al. Carbohydrate intake and multiple sprint sports: with special reference to football (soccer). Int J Sports Med. 1999;20(1):48–52.PubMedGoogle Scholar
  108. 108.
    Coggan A, Coyle E. Effect of carbohydrate feedings during high-intensity exercise. J Appl Physiol. 1988;65(4):1703–9.PubMedGoogle Scholar
  109. 109.
    Nicholas C, Nuttall F, Williams C. The Loughborough Intermittent Shuttle Test: a field test that simulates the activity pattern of soccer. J Sports Sci. 2000;18(2):97–104.PubMedGoogle Scholar
  110. 110.
    Nicholas CW, Williams C, Lakomy HK, Phillips G, Nowitz A. Influence of ingesting a carbohydrate-electrolyte solution on endurance capacity during intermittent, high-intensity shuttle running. J Sports Sci. 1995;13(4):283–90.PubMedGoogle Scholar
  111. 111.
    Davis J, Jackson D, Broadwell M, et al. Carbohydrate drinks delay fatigue during intermittent, high-intensity cycling in active men and women. Int J Sport Nutr. 1997;7(4):261–73.PubMedGoogle Scholar
  112. 112.
    Davis J, Welsh R, Alerson N. Effects of carbohydrate and chromium ingestion during intermittent high-intensity exercise to fatigue. Int J Sport Nutr Exerc Metab. 2000;10(4):476–85.PubMedGoogle Scholar
  113. 113.
    Davis J, Welsh R, De Volve K, et al. Effects of branched-chain amino acids and carbohydrate on fatigue during intermittent, high-intensity running. Int J Sports Med. 1999;20(5):309–14.PubMedGoogle Scholar
  114. 114.
    Nicholas C, Tsintzas K, Boobis L, et al. Carbohydrate-electrolyte ingestion during intermittent high-intensity running. Med Sci Sports Exerc. 1999;31(9):1280–6.PubMedGoogle Scholar
  115. 115.
    Welsh R, Davis J, Burke J, et al. Carbohydrates and physical/mental performance during intermittent exercise to fatigue. Med Sci Sports Exerc. 2002;34(4):723–31.PubMedGoogle Scholar
  116. 116.
    Patterson S, Gray S. Carbohydrate-gel supplementation and endurance performance during intermittent high-intensity shuttle running. Int J Sport Nutr Exerc Metab. 2007;17(5):445–555.PubMedGoogle Scholar
  117. 117.
    Foskett A, Williams C, Boobis L, et al. Carbohydrate availability and muscle energy metabolism during intermittent running. Med Sci Sports Exerc. 2008;40(1):96–103.PubMedGoogle Scholar
  118. 118.
    Davison G, McClean C, Brown J, et al. The effects of ingesting a carbohydrate-electrolyte beverage 15 minutes prior to high-intensity exercise performance. Res Sports Med. 2008;16(3):155–66.PubMedGoogle Scholar
  119. 119.
    Leatt P, Jacobs I. Effect of glucose polymer ingestion on glycogen depletion during a soccer match. Can J Sport Sci. 1989;14(2):112–6.PubMedGoogle Scholar
  120. 120.
    Carling C, Bloomfield J, Nelsen L, et al. The role of motion analysis in elite soccer: contemporary performance measurement techniques and work rate data. Sports Med. 2008;38(10):839–62.PubMedGoogle Scholar
  121. 121.
    Winnick J, Davis J, Welsh R, et al. Carbohydrate feedings during team sport exercise preserve physical and CNS function. Med Sci Sports Exerc. 2005;37(2):306–15.PubMedGoogle Scholar
  122. 122.
    Ali A, Williams C, Nicholas C, et al. The influence of carbohydrate-electrolyte ingestion on soccer skill performance. Med Sci Sports Exerc. 2007;39(11):1969–76.PubMedGoogle Scholar
  123. 123.
    Utter A, Kang J, Nieman D, et al. Carbohydrate attenuates perceived exertion during intermittent exercise and recovery. Med Sci Sports Exerc. 2007;39(5):880–5.PubMedGoogle Scholar
  124. 124.
    Russell M, Benton D, Kingsley M. Influence of carbohydrate supplementation on skill performance during a soccer match simulation. J Sci Med Sport. 2012;15:348–54.PubMedGoogle Scholar
  125. 125.
    Currell K, Conway S, Jeukendrup A. Carbohydrate ingestion improves performance of a new reliable test of soccer performance. Int J Sport Nutr Exerc Metab. 2009;19(1):34–46.PubMedGoogle Scholar
  126. 126.
    Vergauwen L, Brouns F, Hespel P. Carbohydrate supplementation improves stroke performance in tennis. Med Sci Sports Exerc. 1998;30(8):1289–95.PubMedGoogle Scholar
  127. 127.
    Clarke N, Drust B, MacLaren D, et al. Strategies for hydration and energy provision during soccer-specific exercise. Int J Sport Nutr Exerc Metab. 2005;15(6):625–40.PubMedGoogle Scholar
  128. 128.
    Clarke N, Drust B, Maclaren D, et al. Fluid provision and metabolic responses to soccer-specific exercise. Eur J Appl Physiol. 2008;104(6):1069–77.PubMedGoogle Scholar
  129. 129.
    Leiper J, Prentice A, Wrightson C, et al. Gastric emptying of a carbohydrate-electrolyte drink during a soccer match. Med Sci Sports Exerc. 2001;33(11):1932–8.PubMedGoogle Scholar
  130. 130.
    Burke L, Cox G. The complete guide to food for sports performance. 3rd ed. Sydney: Allen and Unwin; 2010.Google Scholar
  131. 131.
    Mujika I, Burke L. Nutrition in Team Sports. Ann Nutr Metab. 2010;57(suppl 2):26–35.Google Scholar
  132. 132.
    Leiper J, Broad N, Maughan R. Effect of intermittent high-intensity exercise on gastric emptying in man. Med Sci Sports Exerc. 2001;33(8):1270.PubMedGoogle Scholar
  133. 133.
    Bosch A, Weltan S, Dennis S, et al. Fuel substrate turnover and oxidation and glycogen sparing with carbohdyrate ingestion in non-carbohydrate-loaded cyclists. Pflugers Arch. 1996;432(6):1003–10.PubMedGoogle Scholar
  134. 134.
    Costill D, Sherman W, Fink W, et al. The role of dietary carbohydrates in muscle glycogen resynthesis after strenuous running. Am J Clin Nutr. 1981;34(9):1831–6.PubMedGoogle Scholar
  135. 135.
    Casey A, Short A, Hultman E, et al. Glycogen resynthesis in human muscle fibre types following exercise-induced glycogen depletion. J Physiol. 1995;483(1):265–71.PubMedGoogle Scholar
  136. 136.
    Keizer H, Kuipers H, van Kranenburg G. Influence of liquid and solid meals on muscle glycogen resynthesis, plasma fuel hormone response, and maximal physical working capacity. Int J Sports Med. 1987;8:99–104.PubMedGoogle Scholar
  137. 137.
    Kochan R, Lamb D, Lutz S, et al. Glycogen synthase activation in human skeletal muscle: effects of diet and exercise. Am J Physiol. 1979;236(6):E660–6.PubMedGoogle Scholar
  138. 138.
    Parkin J, Carey M, Martin I, et al. Muscle glycogen storage following prolonged exercise: effect of timing of ingestion of high glycemic index food. Med Sci Sports Exerc. 1997;29(2):220–4.PubMedGoogle Scholar
  139. 139.
    Nilsson L, Hultman E. Liver and muscle glycogen in man after glucose and fructose infusion. Scand J Clin Lab Invest. 1974;33(1):5–10.PubMedGoogle Scholar
  140. 140.
    Décombaz J, Jentjens R, Ith M, et al. Fructose and galactose enhance post-exercise human liver glycogen synthesis. Med Sci Sports Exerc. 2011;43:1964–1971.Google Scholar
  141. 141.
    Casey A, Mann R, Banister K, et al. Effect of carbohydrate ingestion on glycogen resynthesis in human liver and skeletal muscle measured by 13C MRS. Am J Physiol Endocrinol Metab. 2000;278(1):E65–75.PubMedGoogle Scholar
  142. 142.
    Moriarty K, McIntyre D, Bingham K, et al. Glycogen resynthesis in liver and muscle after exercise: measurement of teh rate of resyntehsis by 13C magnetic resonance spectroscopy. MAGMA. 1994;2(3):429–32.Google Scholar
  143. 143.
    Conlee R, Lawler R, Ross P. Effects of glucose or fructose feeding on glycogen repletion in muscle and liver after exercise or fasting. Ann Nutr Metab. 1987;31(2):126–32.PubMedGoogle Scholar
  144. 144.
    McGuinness O, Cherrington A. Effects of fructose on hepatic glucose metabolism. Curr Opin Clin Nutr Metab Care. 2003;6(4):441–8.PubMedGoogle Scholar
  145. 145.
    Blom P, Hostmark A, Vaage O, et al. Effect of different post-exercise sugar diets on the rate of muscle glycogen synthesis. Med Sci Sports Exerc. 1987;19(5):491–6.PubMedGoogle Scholar
  146. 146.
    Ivy J, Lee M, Brozinick J, et al. Muscle glycogen storage after different amounts of carbohydrate ingestion. J Appl Physiol. 1988;65(5):2018–23.PubMedGoogle Scholar
  147. 147.
    van Loon L, Saris W, Kruijshoop M, et al. Maximizing postexercise muscle glycogen synthesis: Carbohydrate supplementation and the application of amino acid or protein hydrolysate mixtures. Am J Clin Nutr. 2000;72(1):106–11.PubMedGoogle Scholar
  148. 148.
    Ivy J. Glycogen resynthesis after exercise: effect of carbohydrate intake. Int J Sports Med. 1988;19:142–5.Google Scholar
  149. 149.
    Goodyear L, Hirshman M, King P, et al. Skeletal muscle plasma membrane glucose transport and glucose transporters after exercise. J Appl Physiol. 1990;68(1):193–8.PubMedGoogle Scholar
  150. 150.
    Ivy J, Katz A, Cutler C, et al. Muscle glycogen synthesis after exercise: effect of time of carbohydrate ingestion. J Appl Physiol. 1988;64(4):1480–5.PubMedGoogle Scholar
  151. 151.
    Jentjens R, van Loon L, Mann C, et al. Addition of protein and amino acids to carbohydrates does not enhance postexercise muscle glycogen synthesis. J Appl Physiol. 2001;91(2):839–46.PubMedGoogle Scholar
  152. 152.
    van Hall G, Shirreffs S, Calbet J. Muscle glycogen resynthesis during recovery from cycle exercise: no effect of additional protein ingestion. J Appl Physiol. 2000;88(5):1631–6.PubMedGoogle Scholar
  153. 153.
    Piehl Aulin K, Söderlund K, Hultman E. Muscle glycogen resynthesis rate in humans after supplementation of drinks containing carbohydrates with low and high molecular masses. Eur J Appl Physiol. 2000;81(4):346–51.Google Scholar
  154. 154.
    Howarth KR, Moreau NA, Phillips SM, et al. Coingestion of protein with carbohydrate during recovery from endurance exercise stimulates skeletal muscle protein synthesis in humans. J Appl Physiol. 2009;106(4):1394–402.PubMedGoogle Scholar
  155. 155.
    van Loon L, Kruijshoop M, Verhagen H, et al. Ingestion of protein hydrolysate and amino acid–carbohydrate mixtures increases postexercise plasma insulin responses in men. J Nutr. 2000;130(10):2508–13.PubMedGoogle Scholar
  156. 156.
    van Loon L, Saris W, Verhagen H, et al. Plasma insulin responses after ingestion of different amino acid or protein mixtures with carbohydrate. Am J Clin Nutr. 2000;72(1):96–105.PubMedGoogle Scholar
  157. 157.
    Rabinowitz D, Merimee T, Maffezzoli R, et al. Patterns of hormonal release after glucose, protein, and glucose plus protein. Lancet. 1966;2(7461):454–6.PubMedGoogle Scholar
  158. 158.
    Cartee G, Young D, Sleeper M, et al. Prolonged increase in insulin-stimulated glucose transport in muscle after exercise. Am J Physiol. 1989;256:494–9.Google Scholar
  159. 159.
    Jentjens R, Jeukendrup A. Determinants of post-exercise glycogen synthesis during short-term recovery. Sports Med. 2003;33(2):117–44.PubMedGoogle Scholar
  160. 160.
    Wallberg-Henriksson H, Constable S, Young D, et al. Glucose transport into rat skeletal muscle: interaction between exercise and insulin. J Appl Physiol. 1988;65(2):909–13.PubMedGoogle Scholar
  161. 161.
    Berardi J, Price T, Noreen E, et al. Postexercise muscle glycogen recovery enhanced with a carbohydrate-protein supplement. Med Sci Sports Exerc. 2006;38(6):1106–13.PubMedGoogle Scholar
  162. 162.
    Ivy J, Goforth H, Damon B, et al. Early postexercise muscle glycogen recovery is enhanced with a carbohydrate-protein supplement. J Appl Physiol. 2002;93:1337–44.PubMedGoogle Scholar
  163. 163.
    Zawadzki K, Yaspelkis B, Ivy J. Carbohydrate–protein complex increases the rate of muscle glycogen storage after exercise. J Appl Physiol. 1992;72(5):1854–9.PubMedGoogle Scholar
  164. 164.
    Beelen M, van Kranenburg J, Senden J, et al. Impact of caffeine and protein on postexercise muscle glycogen synthesis. Med Sci Sports Exerc. 2012;44(4):692–700.PubMedGoogle Scholar
  165. 165.
    Reed M, Brozinick J, Lee M, et al. Muscle glycogen storage postexercise: effect of mode of carbohydrate administration. J Appl Physiol. 1989;88(2):386–92.Google Scholar
  166. 166.
    Van Den Bergh A, Houtman S, Heerschap A, et al. Muscle glycogen recovery after exercise during glucose and fructose intake monitored by 13C-NMR. J Appl Physiol. 1996;81(4):1495–500.Google Scholar
  167. 167.
    Fujisawa T, Mulligan K, Wada L, et al. The effect of exercise on fructose absorption. Am J Clin Nutr. 1993;58(1):75–9.PubMedGoogle Scholar
  168. 168.
    Henry R, Crapo P, Thorburn A. Current issues in fructose metabolism. Annu Rev Nutr. 1991;11:21–9.PubMedGoogle Scholar
  169. 169.
    Mayes P. Intermediary metabolism of fructose. Am J Clin Nutr. 1993;58:754S–65S.PubMedGoogle Scholar
  170. 170.
    Wallis G, Hulston C, Mann C, et al. Postexercise muscle glycogen synthesis with combined glucose and fructose ingestion. Med Sci Sports Exerc. 2008;40(10):1789–94.PubMedGoogle Scholar
  171. 171.
    Jeukendrup A. Nutrition for endurance sports: marathon, triathlon, and road cycling. J Sports Sci. 2011;29(Suppl 1):S91–9.PubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2013

Authors and Affiliations

  1. 1.Department of Human Movement Sciences, Faculty of Health, Medicine and Life Sciences, NUTRIM School for Nutrition, Toxicology and MetabolismMaastricht University Medical Centre+MaastrichtThe Netherlands

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