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Sports Medicine

, Volume 40, Issue 11, pp 941–959 | Cite as

Short-Term Recovery from Prolonged Exercise

Exploring the Potential for Protein Ingestion to Accentuate the Benefits of Carbohydrate Supplements
  • James A. Betts
  • Clyde Williams
Review Article

Abstract

This review considers aspects of the optimal nutritional strategy for recovery from prolonged moderate to high intensity exercise. Dietary carbohydrate represents a central component of post-exercise nutrition. Therefore, carbohydrate should be ingested as early as possible in the post-exercise period and at frequent (i.e. 15- to 30-minute) intervals throughout recovery to maximize the rate of muscle glycogen resynthesis. Solid and liquid carbohydrate supplements or whole foods can achieve this aim with equal effect but should be of high glycaemic index and ingested following the feeding schedule described above at a rate of at least 1 g/kg/h in order to rapidly and sufficiently increase both blood glucose and insulin concentrations throughout recovery. Adding ≥0.3 g/kg/h of protein to a carbohydrate supplement results in a synergistic increase in insulin secretion that can, in some circumstances, accelerate muscle glycogen resynthesis. Specifically, if carbohydrate has not been ingested in quantities sufficient to maximize the rate of muscle glycogen resynthesis, the inclusion of protein may at least partially compensate for the limited availability of ingested carbohydrate. Some studies have reported improved physical performance with ingestion of carbohydrate-protein mixtures, both during exercise and during recovery prior to a subsequent exercise test. While not all of the evidence supports these ergogenic benefits, there is clearly the potential for improved performance under certain conditions, e.g. if the additional protein increases the energy content of a supplement and/or the carbohydrate fraction is ingested at below the recommended rate. The underlying mechanism for such effects may be partly due to increased muscle glycogen resynthesis during recovery, although there is varied support for other factors such as an increased central drive to exercise, a blunting of exercise-induced muscle damage, altered metabolism during exercise subsequent to recovery, or a combination of these mechanisms.

Keywords

Muscle Glycogen Subsequent Exercise Glycogen Resynthesis Carbohydrate Supplement Muscle Glycogen Concentration 
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

Acknowledgements

The authors’ studies which inform this review were funded by GlaxoSmithKline, who approved submission of this manuscript. The authors have no conflicts of interest that are directly relevant to the content of this review.

References

  1. 1.
    Gollnick PD, Piehl K, Saubert CW, et al. Diet, exercise, and glycogen changes in human muscle fibres. J ApplPhysiol 1972; 33 (4): 421–5PubMedGoogle Scholar
  2. 2.
    Hermansen L, Hultman E, Saltin B. Muscle glycogen during prolonged severe exercise. Acta Physiol Scand 1967; 71: 129–39PubMedCrossRefGoogle Scholar
  3. 3.
    Ahlborg B, Bergstrom J, Ekelund L, et al. Muscle glycogen and muscle electrolytes during prolonged physical exercise. Acta Physiol Scand 1967; 70: 129–42CrossRefGoogle Scholar
  4. 4.
    Bergstrom J, Hermansen L, Hultman E, et al. Diet, muscle glycogen and physical performance. Acta Physiol Scand 1967; 71: 140–50PubMedCrossRefGoogle Scholar
  5. 5.
    Nicholas CW, Green PA, Hawkins RD, et al. Carbohydrate intake and recovery of intermittent running capacity. Int J Sport Nutr 1997; 7 (4): 251–60PubMedGoogle Scholar
  6. 6.
    Burke LM. New issues in training and nutrition: train low, compete high? Curr Sports Med Rep 2007; 6 (3): 137–8PubMedCrossRefGoogle Scholar
  7. 7.
    Battram DS, Shearer J, Robinson D, et al. Caffeine ingestion does not impede the resynthesis of proglycogen andmacroglycogen after prolonged exercise and carbohydratesupplementation in humans. J Appl Physiol 2004; 96 (3): 943–50PubMedCrossRefGoogle Scholar
  8. 8.
    Berardi JM, Price TB, Noreen EE, et al. Postexercise muscle glycogen recovery enhanced with a carbohydrate protein supplement. Med Sci Sports Exerc 2006; 38 (6): 1106–13PubMedCrossRefGoogle Scholar
  9. 9.
    Betts JA, Williams C, Boobis L, et al. Increased carbohydrate oxidation after ingesting carbohydrate with addedprotein. Med Sci Sports Exerc 2008; 40 (5): 903–12PubMedCrossRefGoogle Scholar
  10. 10.
    Blom CS, Hostmark AT, Vaage O, et al. Effect of different post-exercise sugar diets on the rate of muscle glycogensynthesis. Med Sci Sports Exerc 1987; 19 (5): 491–6PubMedGoogle Scholar
  11. 11.
    Blom CS. Post-exercise glucose uptake and glycogen synthesis in human muscle during oral or i.v. glucose intake. Eur J Appl Physiol 1989; 59 (5): 327–33CrossRefGoogle Scholar
  12. 12.
    Carrithers JA, Williamson DL, Gallagher PM, et al. Effects of postexercise carbohydrate-protein feedings onmuscleglycogen restoration. J Appl Physiol 2000; 88 (6): 1976–82PubMedGoogle Scholar
  13. 13.
    Casey A, Mann R, Banister K, et al. Effect of carbohydrate ingestion on glycogen resynthesis in human liver andskeletal muscle, measured by 13C MRS. Am J Physiol 2000; 278: E65–75Google Scholar
  14. 14.
    Casey A, Short AH, Hultman E, et al. Glycogen resynthesis in human muscle fibre types following exercise-inducedglycogen depletion. J Physiol (Lond) 1995; 483 (1): 265–71Google Scholar
  15. 15.
    De Bock K, Richter EA, Russell AP, et al. Exercise in the fasted state facilitates fibre type-specific intramyocellularlipid breakdown and stimulates glycogen resynthesis inhumans. J Physiol (Lond) 2005; 564 (2): 649–60CrossRefGoogle Scholar
  16. 16.
    Doyle JA, Sherman WM, Strauss RL. Effects of eccentric and concentric exercise on muscle glycogen replenishment. J Appl Physiol 1993; 74 (4): 1848–55PubMedGoogle Scholar
  17. 17.
    Howarth KR, Moreau NA, Phillips SM, et al. Coingestion of protein with carbohydrate during recovery from enduranceexercise stimulates skeletal muscle protein synthesisin humans. J Appl Physiol 2009; 106 (4): 1394–402PubMedCrossRefGoogle Scholar
  18. 18.
    Ivy JL, Katz AL, Cutler CL, et al. Muscle glycogen synthesis after exercise: effect of time of carbohydrate ingestion. J Appl Physiol 1988; 64 (4): 1480–5PubMedGoogle Scholar
  19. 19.
    Ivy JL, Lee MC, Brozinick Jr JT, et al. Muscle glycogen storage after different amounts of carbohydrate ingestion. J Appl Physiol 1988; 65 (5): 2018–23PubMedGoogle Scholar
  20. 20.
    Jentjens RLPG, van Loon LJC, Mann CH, et al. Addition of protein and amino acids to carbohydrates does notenhance postexercise muscle glycogen synthesis. J Appl Physiol 2001; 91 (2): 839–46PubMedGoogle Scholar
  21. 21.
    Maehlum S, Felig P, Wahren J. Splanchnic glucose and muscle glycogen metabolism after glucose feeding duringpostexercise recovery. Am J Physiol 1978; 235 (3): E255–260PubMedGoogle Scholar
  22. 22.
    McCoy M, Proietto J, Hargreaves M. Skeletal muscle GLUT-4 and postexercise muscle glycogen storage inhumans. J Appl Physiol 1996; 80 (2): 411–5PubMedGoogle Scholar
  23. 23.
    Pedersen DJ, Lessard SJ, Coffey VG, et al. High rates of muscle glycogen resynthesis after exhaustive exercisewhen carbohydrate is co-ingested with caffeine. J Appl Physiol 2008; 105 (1): 7–13PubMedCrossRefGoogle Scholar
  24. 24.
    Piehl Aulin K, Soderlund K, Hultman E. Muscle glycogen resynthesis rate in humans after supplementation ofdrinks containing carbohydrates with low and high molecularmasses. Eur J Appl Physiol 2000; 81: 346–51PubMedCrossRefGoogle Scholar
  25. 25.
    Price TB, Laurent D, Petersen KF, et al. Glycogen loading alters muscle glycogen resynthesis after exercise. J Appl Physiol 2000; 88: 698–704PubMedGoogle Scholar
  26. 26.
    Reed MJ, Brozinick Jr JT, Lee MC, et al. Muscle glycogen storage postexercise: effect of mode of carbohydrate administration. J Appl Physiol 1989; 66 (2): 720–6PubMedGoogle Scholar
  27. 27.
    Roy BD, Tarnopolsky MA. Influence of differing macronutrient intakes on muscle glycogen resynthesis after resistanceexercise. J Appl Physiol 1998; 84 (3): 890–6PubMedGoogle Scholar
  28. 28.
    Ruby BC, Gaskill SE, Slivka D, et al. The addition of fenugreek extract (Trigonella foenum-graecum) to glucosefeeding increases muscle glycogen resynthesis after exercise. Amino Acids 2005; 28 (1): 71–6PubMedCrossRefGoogle Scholar
  29. 29.
    Shearer J, Wilson RJ, Battram DS, et al. Increases in glycogenin and glycogenin mRNA accompany glycogen resynthesisin human skeletal muscle. Am J Physiol 2005; 289: E508–14Google Scholar
  30. 30.
    Slivka D, Cuddy J, Hailes W, et al. Glycogen resynthesis and exercise performance with the addition of fenugreekextract (4-hydroxyisoleucine) to post-exercise carbohydratefeeding. Amino Acids 2008; 35 (2): 439–44PubMedCrossRefGoogle Scholar
  31. 31.
    Tarnopolsky MA, Bosman M, MacDonald JR, et al. Postexercise protein-carbohydrate and carbohydratesupplements increase muscle glycogen in men and women. J Appl Physiol 1997; 83 (6): 1877–83PubMedGoogle Scholar
  32. 32.
    Tsintzas K, Williams C, Boobis L, et al. Effect of carbohydrate feeding during recovery from prolonged runningon muscle glycogen metabolism during subsequent exercise. Int J Sports Med 2003; 6: 452–8Google Scholar
  33. 33.
    van Hall G, Saris WHM, van de Schoor PAI, et al. The effect of free glutamine and peptide ingestion on the rateof muscle glycogen resynthesis in man. Int J Sports Med 2000; 21: 25–30PubMedCrossRefGoogle Scholar
  34. 34.
    van Hall G, Shirreffs SM, Calbet JA. Muscle glycogen resynthesis during recovery from cycle exercise: no effect ofadditional protein ingestion. J Appl Physiol 2000; 88 (5): 1631–6PubMedGoogle Scholar
  35. 35.
    van Loon LJ, Saris WH, Kruijshoop M, et al. Maximizing postexercise muscle glycogen synthesis: carbohydratesupplementation and the application of amino acid orprotein hydrolysate mixtures. Am J Clin Nutr 2000; 72 (1): 106–11PubMedGoogle Scholar
  36. 36.
    Wallis GA, Hulston CJ, Mann CH, et al. Postexercise muscle glycogen synthesis with combined glucose andfructose ingestion. Med Sci Sports Exerc 2008; 40 (10): 1789–94PubMedCrossRefGoogle Scholar
  37. 37.
    Yaspelkis BB, Ivy JL. The effect of a carbohydrate-arginine supplement on postexercise carbohydrate metabolism. IntJ Sport Nutr 1999; 9 (3): 241–50Google Scholar
  38. 38.
    Zachwieja JJ, Costill DL, Pascoe DD, et al. Influence of muscle glycogen depletion on the rate of resynthesis. Med Sci Sports Exerc 1991; 23 (1): 44–8PubMedGoogle Scholar
  39. 39.
    Zawadzki KM, Yaspelkis 3rd BB, Ivy JL. Carbohydrateprotein complex increases the rate of muscle glycogenstorage after exercise. J Appl Physiol 1992; 72 (5): 1854–9PubMedGoogle Scholar
  40. 40.
    Fallowfield JL, Williams C, Singh R. The influence of ingesting a carbohydrate-electrolyte beverage during4 hours of recovery on subsequent endurance capacity. IntJ Sport Nutr 1995; 5: 285–99Google Scholar
  41. 41.
    Cartee GD, Young DA, Sleeper MD, et al. Prolonged increase in insulin-stimulated glucose transport in muscleafter exercise. Am J Physiol 1989; 256 (4): E494–9PubMedGoogle Scholar
  42. 42.
    Young DA, Wallberg-Henriksson H, Sleeper MD, et al. Reversal of the exercise induced increase in muscle permeabilityto glucose. Am J Physiol 1987; 253: E331–5PubMedGoogle Scholar
  43. 43.
    Goodyear LJ, King PA, Hirshman MF, et al. Contractile activity increases plasma membrane glucose transportersin absence of insulin. Am J Physiol 1990; 258: E667–72PubMedGoogle Scholar
  44. 44.
    Kiens B, Raben AB, Valeur A-K, et al. Benefit of dietary simple carbohydrates on the early postexercise muscleglycogen repletion in male runners [abstract]. Med Sci Sports Exerc 1990; 22 (2): S89Google Scholar
  45. 45.
    Burke LM, Collier GR, Hargreaves M. Muscle glycogen storage after prolonged exercise: effect of the glycaemicindex of carbohydrate feedings. J Appl Physiol 1993; 75 (2): 1019–23PubMedGoogle Scholar
  46. 46.
    Nilsson LH, Hultman E. Liver and muscle glycogen in man after glucose and fructose infusion. Scand J Clin Lab Invest 1974; 33 (1): 5–10PubMedCrossRefGoogle Scholar
  47. 47.
    Jentjens RL, Jeukendrup AE. High rates of exogenous carbohydrate oxidation from a mixture of glucose andfructose ingested during prolonged cycling exercise. Br JNutr 2005; 93 (4): 485–92CrossRefGoogle Scholar
  48. 48.
    Wu CL, Williams C. A low glycemic index meal before exercise improves endurance running capacity in men. IntJ Sport Nutr Ex Met 2006; 16 (5): 510–27Google Scholar
  49. 49.
    Stevenson E, Williams C, McComb G, et al. Improved recovery from prolonged exercise following the consumptionof low glycemic index carbohydrate meals. Int J Sport Nutr Ex Met 2005; 15 (4): 333–49Google Scholar
  50. 50.
    Erith S, Williams C, Stevenson E, et al. The effect of high carbohydrate meals with different glycemic indices on recoveryof performance during prolonged intermittenthigh-intensity shuttle running. Int J Sport Nutr Ex Met 2006; 16 (4): 393–404Google Scholar
  51. 51.
    Keizer HA, Kuipers H, van Kranenburg G, et al. Influence of liquid and solid meals on muscle glycogen resynthesis,plasma fuel hormone response, and maximal physicalworking capacity. Int J Sports Med 1987; 8 (2): 99–104PubMedCrossRefGoogle Scholar
  52. 52.
    Moodley D, Noakes TD, Bosch AN, et al. Oxidation of exogenous carbohydrate during prolonged exercise: theeffects of the carbohydrate type and its concentration. EurJ Appl Physiol 1992; 64 (4): 328–34CrossRefGoogle Scholar
  53. 53.
    Rehrer NJ, Wagenmakers AJ, Beckers EJ, et al. Gastric emptying, absorption, and carbohydrate oxidation duringprolonged exercise. J Appl Physiol 1992; 72 (2): 468–75PubMedGoogle Scholar
  54. 54.
    Rowlands DS, Wallis GA, Shaw C, et al. Glucose polymer molecular weight does not affect exogenous carbohydrateoxidation. Med Sci Sports Exerc 2005; 37 (9): 1510–6PubMedCrossRefGoogle Scholar
  55. 55.
    Stephens FB, Roig M, Armstrong G, et al. Post-exercise ingestion of a unique, high molecular weight glucose polymersolution improves performance during a subsequentbout of cycling exercise. J Sports Sci 2008; 26 (2): 149–54PubMedCrossRefGoogle Scholar
  56. 56.
    Parkin JAM, Carey MF, Martin IK, et al. Muscle glycogen storage following prolonged exercise: effect of timing ofingestion of high glycemic index food. Med Sci Sports Exerc 1997; 29 (2): 220–4PubMedCrossRefGoogle Scholar
  57. 57.
    Laurent D, Hundal RS, Dresner A, et al. Mechansim of muscle glycogen autoregulation in humans. Am J Physiol 2000; 278: E663–8Google Scholar
  58. 58.
    Watt MJ, Heigenhauser GJF, Dyck DJ, et al. Intramuscular triacylglycerol, glycogen and acetyl group metabolism during 4 h of moderate exercise in man. J Physiol (Lond) 2002; 541 (3): 969–78CrossRefGoogle Scholar
  59. 59.
    Jentjens R, Jeukendrup AE. Determinants of post-exercise glycogen synthesis during short-term recovery. Sports Med 2003; 33 (2): 117–44PubMedCrossRefGoogle Scholar
  60. 60.
    Floyd Jr JC, Fajans SS, Conn JW, et al. Stimulation of insulin secretion by amino acids. J Clin Invest 1966; 45 (9): 1487–501PubMedCrossRefGoogle Scholar
  61. 61.
    Rabinowitz D, Merimee TJ, Maffezzoli R, et al. Patterns of hormonal release after glucose, protein, and glucose plusprotein. Lancet 1966; 2 (7461): 454–6PubMedCrossRefGoogle Scholar
  62. 62.
    Floyd Jr JC, Fajans SS, Pek S, et al. Synergistic effect of essential amino acids and glucose upon insulin secretionin man. Diabetes 1970; 19 (2): 109–15PubMedGoogle Scholar
  63. 63.
    Floyd Jr JC, Fajans SS, Pek S, et al. Synergistic effect of certain amino acid pairs upon insulin secretion in man. Diabetes 1970; 19 (2): 102–8PubMedGoogle Scholar
  64. 64.
    van Loon LJ, Saris WH, Verhagen H, et al. Plasma insulin responses after ingestion of different amino acid or proteinmixtures with carbohydrate. Am J Clin Nutr 2000; 72 (1): 96–105PubMedGoogle Scholar
  65. 65.
    Robinson TM, Sewell DA, Greenhaff PL. L-Arginine ingestion after rest and exercise: effects on glucose disposal. Med Sci Sports Exerc 2003; 35 (8): 1309–15PubMedCrossRefGoogle Scholar
  66. 66.
    Gannon MC, Nuttall JA, Nuttall FQ. Oral arganine does not stimulate an increase in insulin concentration but delaysglucose disposal. Am J Clin Nutr 2002; 76: 1016–22PubMedGoogle Scholar
  67. 67.
    van Loon LJC, Kruijshoop M, Verhagen H, et al. Ingestion of protein hydrolysate and amino acid-carbohydratemixtures increases postexercise plasma insulin responsesin men. J Nutr 2000; 130 (10): 2508–13PubMedGoogle Scholar
  68. 68.
    Spiller GA, Jensen CD, Pattison TS, et al. Effect of protein dose on serum glucose and insulin response to sugars. AmJ Clin Nutr 1987; 46 (3): 474–80Google Scholar
  69. 69.
    Thomas JE. Mechanics and regulation of gastric emptying. Physiol Rev 1957; 37: 453–74PubMedGoogle Scholar
  70. 70.
    Kaastra B, Manders RJF, van Breda E, et al. Effects of increasing insulin secretion on acute postexercise bloodglucose disposal. Med Sci Sports Exerc 2006; 38 (2): 268–75PubMedCrossRefGoogle Scholar
  71. 71.
    Rotman S, Slotboom J, Kreis R, et al. Muscle glycogen recovery after exercise measured by 13C-magnetic resonancespectroscopy in humans: effect of nutritional solutions. MAGMA 2000; 11 (3): 114–21PubMedCrossRefGoogle Scholar
  72. 72.
    Betts JA, Stevenson E, Williams C, et al. Recovery of endurance running capacity: effect of carbohydrate-proteinmixtures. Int J Sport Nutr Ex Met 2005; 15 (6): 590–609Google Scholar
  73. 73.
    Betts JA, Williams C, Duffy K, et al. The influence of carbohydrate and protein ingestion during recovery fromprolonged exercise on subsequent endurance performance. J Sports Sci 2007; 25 (13): 1449–60PubMedCrossRefGoogle Scholar
  74. 74.
    Kammer L, Ding Z, Wang B, et al. Cereal and nonfat milk support muscle recovery following exercise. J Int Soc Sports Nutr 2009; 6: 11PubMedCrossRefGoogle Scholar
  75. 75.
    Ivy JL, Goforth HW, Damon BM, et al. Early postexercise muscle glycogen recovery is enhanced with a carbohydrate-protein supplement. J Appl Physiol 2002; 93 (4): 1337–44PubMedGoogle Scholar
  76. 76.
    Ivy JL, Res PT, Sprague RC, et al. Effect of a carbohydrate- protein supplement on endurance performance during exercise of varying intensity. Int J Sport Nutr Ex Met 2003; 13: 382–95Google Scholar
  77. 77.
    Morifuji M, Kanda A, Koga J, et al. Post-exercise carbohydrate plus whey protein hydrolysates supplementationincreases skeletal muscle glycogen level in rats. Amino Acids 2010; 38 (4): 1109–15PubMedCrossRefGoogle Scholar
  78. 78.
    Anthony JC, Anthony TG, Layman DK. Leucine supplementation enhances skeletal muscle recovery in rats followingexercise. J Nutr 1999; 129 (6): 1102–6PubMedGoogle Scholar
  79. 79.
    Wilkinson SB, Kim PL, Armstrong D, et al. Addition of glutamine to essential amino acids and carbohydrate doesnot enhance anabolism in young human males followingexercise. Appl Physiol Nutr Metab 2006; 31 (5): 518–29PubMedCrossRefGoogle Scholar
  80. 80.
    Varnier M, Leese GP, Thompson J, et al. Stimulatory effect of glutamine on glycogen accumulation in human skeletalmuscle. Am J Physiol 1995; 269: E309–15PubMedGoogle Scholar
  81. 81.
    Lam TKT, Carpentier A, Lewis GF, et al. Mechanisms of the free fatty acid-induced increase in hepatic glucoseproduction. Am J Physiol 2003; 284: E863–73Google Scholar
  82. 82.
    Edgerton DS, Ramnanan CJ, Grueter CA, et al. Effects of insulin on the metabolic control of hepatic gluconeogenesisin vivo. Diabetes 2009; 58: 2766–75PubMedCrossRefGoogle Scholar
  83. 83.
    Williams MB, Raven PB, Fogt DL, et al. Effects of recovery beverages on glycogen restoration and enduranceexercise performance. J Strength Cond Res 2003; 17 (1): 12–19PubMedGoogle Scholar
  84. 84.
    Fogt DL, Ivy JL. Effects of post exercise carbohydrateprotein supplement on skeletal muscle glycogen storage[abstract]. Med Sci Sports Exerc 2000; 32: S60Google Scholar
  85. 85.
    Taylor R, Price TB, Rothman DL, et al. Validation of 13C NMR measurement of human skeletal muscle glycogencontent by direct biochemical assay of needle biopsysamples. Magn Reson Med 1992; 27 (1): 13–20PubMedCrossRefGoogle Scholar
  86. 86.
    Costill DL, Pascoe DD, Fink WJ, et al. Impaired muscle glycogen resynthesis after eccentric exercise. J Appl Physiol 1990; 69 (1): 46–50PubMedGoogle Scholar
  87. 87.
    O’Reilly KP, Warhol MJ, Fielding RA, et al. Eccentric exercise induced muscle damage impairs muscle glycogenrepletion. J Appl Physiol 1987; 63 (1): 252–6PubMedGoogle Scholar
  88. 88.
    Asp S, Watkinson A, Oakes ND, et al. Prior eccentric contractions impair maximal insulin action on muscleglucose uptake in the conscious rat. J Appl Physiol 1997; 82 (4): 1327–32PubMedGoogle Scholar
  89. 89.
    Asp S, Daugaard JR, Kristiansen S, et al. Exercise metabolism in human skeletal muscle exposed to prior eccentricexercise. J Physiol (Lond) 1998; 509 (1): 305–13CrossRefGoogle Scholar
  90. 90.
    Terjung RL, Baldwin KM, Winder WW, et al. Glycogen repletion in different types of muscle and in liver afterexhausting exercise. Am J Physiol 1974; 226 (6): 1387–91PubMedGoogle Scholar
  91. 91.
    Saunders MJ, Kane MD, Todd MK. Effects of a carbohydrate- protein beverage on cycling performance andmuscle damage. Med Sci Sports Exerc 2004; 36 (7): 1233–8PubMedCrossRefGoogle Scholar
  92. 92.
    Baty JJ, Hwang H, Ding Z, et al. The effect of a carbohydrate and protein supplement on resistance exercise performance,hormonal response, and muscle damage. J Strength Cond Res 2007; 21 (2): 321–9PubMedGoogle Scholar
  93. 93.
    Cockburn E, Hayes PR, French DN, et al. Acute milkbased protein-CHO supplementation attenuates exerciseinducedmuscle damage. Appl Physiol Nutr Metab 2008; 33 (4): 775–83PubMedCrossRefGoogle Scholar
  94. 94.
    Seifert JG, Kipp RW, Amann M, et al. Muscle damage, fluid ingestion, and energy supplementation during recreationalalpine skiing. Int J Sport Nutr Ex Met 2005; 15 (5): 528–36Google Scholar
  95. 95.
    Valentine RJ, Saunders MJ, Todd MK, et al. Influence of carbohydrate-protein beverage on cycling endurance andindices of muscle disruption. Int J Sport Nutr Ex Met 2008; 18 (4): 363–78Google Scholar
  96. 96.
    Ferguson-Stegall L, McCleave EL, Ding Z, et al. The effect of a low carbohydrate beverage with added protein oncycling endurance performance in trained athletes. J Strength Cond Res. Epub 2010 Aug; 20Google Scholar
  97. 97.
    Luden ND, Saunders MJ, Todd MK. Postexercise carbohydrate- protein-antioxidant ingestion decreases plasmacreatine kinase and muscle soreness. Int J Sport Nutr Ex Met 2007; 17 (1): 109–23Google Scholar
  98. 98.
    Romano-Ely BC, Todd MK, Saunders MJ, et al. Effect of an isocaloric carbohydrate-protein-antioxidant drink oncycling performance. Med Sci Sports Exerc 2006; 38 (9): 1608–16PubMedCrossRefGoogle Scholar
  99. 99.
    Rowlands DS, Thorp RM, Rossler K, et al. Effect of protein- rich feeding on recovery after intense exercise. IntJ Sport Nutr Ex Met 2007; 17 (6): 521–43Google Scholar
  100. 100.
    Saunders MJ, Luden ND, Herrick JE. Consumption of an oral carbohydrate-protein gel improves cycling enduranceand prevents postexercise muscle damage. J Strength Cond Res 2007; 21 (3): 678–84PubMedGoogle Scholar
  101. 101.
    Skillen RA, Testa M, Applegate EA, et al. Effects of an amino acid carbohydrate drink on exercise performanceafter consecutive-day exercise bouts. Int J Sport Nutr Ex Met 2008; 18 (5): 473–92Google Scholar
  102. 102.
    Pritchett K, Bishop P, Pritchett R, et al. Acute effects of chocolate milk and a commercial recovery beverage onpostexercise recovery indices and endurance cycling performance. Appl Physiol Nutr Metab 2009; 34: 1017–22PubMedCrossRefGoogle Scholar
  103. 103.
    Bird SP, Tarpenning KM, Marino FE. Liquid carbohydrate/ essential amino acid ingestion during a short-termbout of resistance exercise suppresses myofibrillar proteindegradation. Metabolism 2006; 55 (5): 570–7PubMedCrossRefGoogle Scholar
  104. 104.
    Green MS, Corona BT, Doyle JA, et al. Carbohydrateprotein drinks do not enhance recovery from exerciseinducedmuscle injury. Int J Sport Nutr Ex Met 2008; 18 (1): 1–18Google Scholar
  105. 105.
    Betts JA, Toone RJ, Stokes KA, et al. Systemic indices of skeletal muscle damage and recovery of muscle functionafter exercise: effect of combined carbohydrate-proteiningestion. Appl Physiol Nutr Metab 2009; 34 (4): 773–84PubMedCrossRefGoogle Scholar
  106. 106.
    Millard-Stafford M, Warren GL, Thomas LM, et al. Recovery from run training: efficacy of a carbohydrateproteinbeverage. Int J Sport Nutr Ex Met 2005; 15 (6): 610–24Google Scholar
  107. 107.
    White JP, Wilson JM, Austin KG, et al. Effect of carbohydrate- protein supplement timing on acute exercise-inducedmuscle damage. J Int Soc Sports Nutr 2008; 5: 5PubMedCrossRefGoogle Scholar
  108. 108.
    Wojcik JR, Wallberg-Rankin J, Smith LL, et al. Comparison of carbohydrate and milk-based beverages on muscledamage and glycogen following exercise. Int J Sport Nutr Ex Met 2001; 11: 406–19Google Scholar
  109. 109.
    Saunders MJ, Moore RW, Kies AK, et al. Carbohydrate and protein hydrolysate coingestions improvement of late-exercise time-trial performance. Int J Sport Nutr Ex Met 2009; 19 (2): 136–49Google Scholar
  110. 110.
    Breen L, Tipton DK, Jeukendrup AE. No effect of carbohydrate- protein on cycling performance and indices ofrecovery. Med Sci Sports Exerc 2010; 42 (6): 1140–8PubMedGoogle Scholar
  111. 111.
    Margaritis I, Tessier F, Verdera F, et al. Muscle enzyme release does not predict muscle function impairment aftertriathlon. J Sports Med Phys Fitness 1999; 39: 133–9PubMedGoogle Scholar
  112. 112.
    Clarkson PM, Hubal MJ. Exercise-induced muscle damage in humans. Am J Phys Med Rehabil 2002; 81 (11): S52–69PubMedCrossRefGoogle Scholar
  113. 113.
    Rowlands DS, Rossler K, Thorp RM, et al. Effect of dietary protein content during recovery from high-intensitycycling on subsequent performance and markers of stress,inflammation, and muscle damage in well-trained men. Appl Physiol Nutr Metab 2008; 33 (1): 39–51PubMedCrossRefGoogle Scholar
  114. 114.
    Levenhagen DK, Carr C, Carlson MG, et al. Postexercise protein intake enhances whole-body and leg protein accretionin humans. Med Sci Sports Exerc 2002; 34 (5): 828–37PubMedCrossRefGoogle Scholar
  115. 115.
    Davis JM. Carbohydrates, branched-chain amino acids, and endurance: the central fatigue hypothesis. Int J Sport Nutr 1995; 5: S29–38PubMedGoogle Scholar
  116. 116.
    Wagenmakers AJM, Coakley JH, Edwards RHT. Metabolism of branched-chain amino acids and ammonia during exercise: clues from McArdle’s disease. Int J Sports Med 1990; 11: S101–13PubMedCrossRefGoogle Scholar
  117. 117.
    Davis JM, Bailey SP, Woods JA, et al. Effects of carbohydrate feedings on plasma free tryptophan and branchedchainamino acids during prolonged cycling. Eur J Appl Physiol 1992; 65 (6): 513–9CrossRefGoogle Scholar
  118. 118.
    Madsen K, MacLean DA, Kiens B, et al. Effects of glucose, glucose plus branched-chain amino acids, or placebo onbike performance over 100 km. J Appl Physiol 1996; 81 (6): 2644–50PubMedGoogle Scholar
  119. 119.
    Dawson KD, Baker DJ, Greenhaff PL, et al. An acute decrease in TCA cycle intermediates does not affect aerobicenergy delivery in contracting rat skeletal muscle. J Physiol(Lond) 2005; 565 (2): 637–43CrossRefGoogle Scholar
  120. 120.
    Gibala MJ. Anaplerosis of the muscle tricarboxylic acid cycle pool during contraction: does size matter? [comment]. J Physiol (Lond) 2003; 548 (Pt2): 334Google Scholar
  121. 121.
    Ghosh AK, Rahaman AA, Singh R. Combination of sago and soy-protein supplementation during endurance cycling exercise and subsequent high-intensity endurancecapacity. Int J Sport Nutr Exerc Metab 2010; 20 (3): 216–23PubMedGoogle Scholar
  122. 122.
    Martinez-Lagunas V, Ding Z, Bernard JR, et al. Added protein maintains efficacy of a low-carbohydrate sportsdrink. J Strength Cond Res 2010; 24 (1): 48–59PubMedCrossRefGoogle Scholar
  123. 123.
    Osterberg KL, Zachwieja JJ, Smith JW. Carbohydrate and carbohydrate + protein for cycling time-trial performance. J Sports Sci 2008; 26 (3): 227–33PubMedCrossRefGoogle Scholar
  124. 124.
    van Essen M, Gibala MJ. Failure of protein to improve time trial performance when added to a sports drink. Med Sci Sports Exerc 2006; 38 (8): 1476–83PubMedCrossRefGoogle Scholar
  125. 125.
    Toone RJ, Betts JA. Isocaloric carbohydrate versus carbohydrate- protein ingestion and cycling time-trial performance. Int J Sport Nutr Ex Met 2010; 20 (1): 34–43Google Scholar
  126. 126.
    Fallowfield JL, Williams C. The influence of a high carbohydrate intake during recovery from prolonged, constantpace running. Int J Sport Nutr 1997; 7: 10–25PubMedGoogle Scholar
  127. 127.
    Wong SH, Williams C. Influence of different amounts of carbohydrate on endurance running capacity followingshort term recovery. Int J Sports Med 2000; 21: 444–52PubMedCrossRefGoogle Scholar
  128. 128.
    Karp JR, Johnston JD, Tecklenburg S, et al. Chocolate milk as a post-exercise recovery aid. Int J Sport Nutr Ex Met 2006; 16: 78–91Google Scholar
  129. 129.
    Berardi JM, Noreen EE, Lemon PW. Recovery from a cycling time trial is enhanced with carbohydrate-proteinsupplementation vs isoenergetic carbohydrate supplementation. J Int Soc Sports Nutr 2008; 5: 24PubMedCrossRefGoogle Scholar
  130. 130.
    Thomas K, Morris P, Stevenson E. Improved endurance capacity following chocolate milk consumption comparedwith 2 commercially available sport drinks. Appl Physiol Nutr Metab 2009; 34 (1): 78–82PubMedCrossRefGoogle Scholar
  131. 131.
    Claassen A, Lambert EV, Bosch AN, et al. Variability in exercise capacity and metabolic response during enduranceexercise after a low carbohydrate diet. Int J Sport Nutr Ex Met 2005; 15: 97–116Google Scholar

Copyright information

© Adis Data Information BV 2010

Authors and Affiliations

  1. 1.Human Physiology Research GroupUniversity of BathBathUK
  2. 2.School of Sport, Exercise and Health SciencesLoughborough UniversityLeicestershireUK

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