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The effects of carbohydrate supplementation during the second of two prolonged cycling bouts on immunoendocrine responses

  • Tzai-Li LiEmail author
  • Michael Gleeson
Original Article

Abstract

The purpose of this study was to examine the effect of carbohydrate (CHO) feeding during the second of two 90-min cycling bouts (EX1 started at 09:00 and EX2 started at 13:30) at 60% \(\dot{V}\hbox{O}_{2\max} \) on leucocyte redistribution, neutrophil degranulation and oxidative burst and plasma IL-6 and stress hormone responses. This study consisted of two trials, which were completed in a counterbalanced order and separated by at least 4 days. Subjects (n=9) consumed a lemon flavoured 10% w/v CHO (glucose) or placebo (PLA) beverage during EX2: 500 ml just before exercise and 250 ml every 20 min during exercise. Venous blood samples were taken 5 min before exercise, immediately post-exercise, and 18-h post-EX2 for both trials. The main findings of this study were that ingestion of CHO compared with PLA during EX2 better maintained plasma glucose concentration, blunted the responses of plasma adrenaline, ACTH, cortisol, GH and IL-6, and attenuated the leukocytosis and monocytosis, but had no effect on neutrophil degranulation and oxidative burst activity. Furthermore, the immunoendocrine disturbances induced by two bouts of prolonged exercise returned to resting values within 18 h. These findings suggest that ingestion of CHO compared with PLA during the second of two bouts of 90-min cycling at 60% \(\dot{V}\hbox{O}_{2\max} \) better maintains plasma glucose, blunts hypothalamic–pituitary–adrenal activation, and attenuates leucocyte trafficking, but does not affect neutrophil function. Furthermore, the disturbances of immunoendocrine responses induced by two bouts of prolonged exercise on the same day recover within 18 h.

Keywords

Leucocyte trafficking Neutrophil degranulation Neutrophil oxidative burst IL-6 Stress hormones 

References

  1. Benschop RJ, Rodriguez-Feuerhahn M, Schedlowski M (1996) Catecholamine-induced leukocytosis: early observations, current research, and future directions. Brain Behav Immun 10:77–91PubMedCrossRefGoogle Scholar
  2. Berkow RL, Dodson RW (1986) Purification and functional evaluation of mature neutrophils from human bone marrow. Blood 68:853–860PubMedGoogle Scholar
  3. Bishop NC, Blannin AK, Walsh NP, Robson PJ, Gleeson M (1999) Nutritional aspects of immunosuppression in athletes. Sports Med 28:151–176PubMedCrossRefGoogle Scholar
  4. Bishop NC, Blannin AK, Walsh NP, Gleeson M (2001) Carbohydrate beverage ingestion and neutrophil degranulation responses following cycling to fatigue at 75% VO2 max. Int J Sports Med 22:226–231PubMedCrossRefGoogle Scholar
  5. Bishop NC, Gleeson M, Nicholas CW, Ali A (2002) Influence of carbohydrate supplementation on plasma cytokine and neutrophil degranulation responses to high intensity intermittent exercise. Int J Sport Nutr Exerc Metab 12:145–156PubMedGoogle Scholar
  6. Blannin AK, Chatwin LJ, Cave R, Gleeson M (1996) Effects of submaximal cycling and long term endurance training on neutrophil phagocytic activity in middle aged men. Br J Sports Med 30:125–129PubMedGoogle Scholar
  7. Blannin AK, Gleeson M, Brooks S, Cave R (1997) The effects of endurance training in the bacterially stimulated degranulation of human neutrophils in vitro. J Sport Sci 15:28Google Scholar
  8. Boyum A, Ronsen O, Tennfjord VA, Tollefsen S, Haugen AH, Opstad PK, Bahr R (2002) Chemiluminescence response of granulocytes from elite athletes during recovery from one or two intense bouts of exercise. Eur J Appl Physiol 88:20–28PubMedCrossRefGoogle Scholar
  9. Costill DL, Hargreaves M (1992) Carbohydrate nutrition and fatigue. Sports Med 13:86–92PubMedGoogle Scholar
  10. Coyle EF, Hagberg JM, Hurley BF, Martin WH, Whsani AA, Holloszy JO (1983) Carbohydrate feeding during prolonged strenuous exercise can delay fatigue. J Appl Physiol 55:230–235PubMedGoogle Scholar
  11. Dill DB, Costill DL (1974) Calculation of percentage changes in volumes of blood, plasma, and red cells in dehydration. J Appl Physiol 37:247–248PubMedGoogle Scholar
  12. Febbraio M, Pedersen BK (2002) Muscle derived interleukin-6 mechanisms for activation and possible biological roles. FASEB J 16:1335–1347PubMedCrossRefGoogle Scholar
  13. Fukatsu K, Sato N, Shimizu H (1996) 50-mile walking race suppresses neutrophil bactericidal function by inducing increases in cortisol and ketone bodies. Life Sci 58:2337–2343PubMedCrossRefGoogle Scholar
  14. Fukuda S, Schmid-Schonbein GW (2002) Centrifugation attenuates the fluid shear response of circulating leukocytes. J Leukoc Biol 72:133–139PubMedGoogle Scholar
  15. Gabriel H, Muller HJ, Urhausen A, Kindermann W (1994) Suppressed PMA-induced oxidative burst and unimpaired phagocytosis of circulating granulocytes one week after a long endurance exercise. Int J Sports Med 15:441–445PubMedGoogle Scholar
  16. Gleeson M (2000) Interleukins and exercise. J Physiol 529:1PubMedCrossRefGoogle Scholar
  17. Gleeson M, Bishop NC (1999) Immunology. In: Maughan RJ (ed) Basic and applied sciences for sports medicine. Butterworth-Heinemann, Oxford, pp 199–236Google Scholar
  18. Gleeson M, Bishop NC (2000) Modification of immune responses to exercise by carbohydrate, glutamine and anti-oxidant supplements. Immunol Cell Biol 78:554–561PubMedCrossRefGoogle Scholar
  19. Gleeson M, Walsh NP, Blannin AK, Robson PJ, Cook L, Donelly AE, Day SH (1998) The effect of severe eccentric exercise-induced muscle damage on plasma elastase, glutamine and zinc concentrations. Eur J Appl Physiol 77:543–546CrossRefGoogle Scholar
  20. Johnson JL, Moore EE, Tamura DY, Zallen G, Biffl WL, Silliman CC (1998) Interleukin-6 augments neutrophil cytotoxic potential via selective enhancement of elastase release. J Surg Res 76:91–94PubMedCrossRefGoogle Scholar
  21. Kappel M, Hansen MB, Diamant M, Jorgensen JOL, Gyhrs A, Pedersen BK (1993) Effects of an acute bolus growth hormone infusion on the human immune system. Horm Metabol Res 25:579–585Google Scholar
  22. Lancaster GI, Jentjen RLPG, Moseley L, Jeukendrup AE, Gleeson M (2003) Effect of pre-exercise carbohydrate ingestion on plasma cytokine, stress hormone, and neutrophil degranulation responses to continuous, high intensity exercise. Int J Sport Nutr Exerc Metab 13:1–18Google Scholar
  23. Losche W, Dressel M, Krause S, Redlich H, Spangenberg P, Heptinstall S (1996) Contact-induced modulation of neutrophil elastase secretion and phagocytic activity by platelets. Blood Coagul Fibrinolysis 7:210–213PubMedCrossRefGoogle Scholar
  24. Mackinnon LT (1999) Advances in exercise immunology. Human Kinetics, ChampaignGoogle Scholar
  25. Mitchell JB, Costill DL, Houmard JA, Flynn MG, Fink WJ, Beltz JD (1990) Influence of carbohydrate ingestion on counterregulatory hormones during prolonged exercise. Int J Sports Med 11:33–36PubMedCrossRefGoogle Scholar
  26. Morozov VI, Pryatkin SA, Kalinski MI, Rogozkin VA (2003) Effect of exercise to exhaustion on myeloperoxidase and lysozyme release from blood neutrophils. Eur J Appl Physiol 89:257–262PubMedCrossRefGoogle Scholar
  27. Mullen PG, Windsor ACJ, Walsh CJ, Fowler AA, Sugerman HJ (1995) Tumor necrosis factor-á and interleukin-6 selectively regulate neutrophil function in vitro. J Surg Res 58:124–130PubMedCrossRefGoogle Scholar
  28. Nakagawa M, Terashima T, D’yachkova Y, Bondy GP, Hogg JC, Van Eeden SF (1998) Glucocorticoid-induced granulocytosis: contribution of marrow release and demargination of intravascular granulocytes. Circulation 98:2307–2313PubMedGoogle Scholar
  29. Nieman DC (1997) Immune response to heavy exertion. J Appl Physiol 82:1385–1394PubMedGoogle Scholar
  30. Nieman DC, Fagoaga OR, Butterworth DE, Warren BJ, Utter A, Davis JM, Henson DA, Nehlsen-Cannarelia SL (1997) Carbohydrate supplementation affects blood granulocyte and monocyte trafficking but not function after 2.5 h of running. Am J Clin Nutr 66:153–159PubMedGoogle Scholar
  31. Ottonello L, Barbera P, Dapino P, Sacchetti C, Dallegri F (1997) Chemoattractant-induced release of elastase by lipopolysaccharide (LPS)-primed neutrophils; inhibitory effect of the anti-inflammatory drug nimesulide. Clin Exp Immunol 110:139–143PubMedCrossRefGoogle Scholar
  32. Parslow TG, Stites DP, Terr AI, Imboden JB (2001) Medical immunology, 10th edn. McGraw-Hill, New YorkGoogle Scholar
  33. Pedersen BK (1999) Exercise and immune function. In: Schedlowski M, Tewes U (eds) Psychoneuroimmunology: an interdisciolinary introduction. Kluwer/Plenum, New York, pp 341–358Google Scholar
  34. Pedersen BK, Hoffman-Goetz L (2000) Exercise and the immune system: regulation, integration, and adaptation. Physiol Rev 80:1055–1081PubMedGoogle Scholar
  35. Prasad K, Chaudhary AK, Kalra J (1991) Oxygen-derived free radicals producing activity and survival of activated polymorphonuclear leukocytes. Mol Cell Biochem 103:51–62PubMedCrossRefGoogle Scholar
  36. Pyne DB (1994) Regulation of neutrophil function during exercise. Sports Med 17:245–258PubMedCrossRefGoogle Scholar
  37. Pyne DB, Baker MS, Smith JA, Telford RD (1996) Exercise and the neutrophil oxidative burst: biological and experimental variability. Eur J Appl Physiol 74:564–571Google Scholar
  38. Robson PJ, Blannin AK, Walsh NP, Castell LM, Gleeson M (1999) Effects of exercise intensity, duration and recovery on in vitro neutrophil function in male athletes. Int J Sports Med 20:128–135PubMedCrossRefGoogle Scholar
  39. Ronsen O, Haug E, Pedersen BK, Bahr R (2001a) Increased neuroendocrine response to a repeated bout of endurance exercise. Med Sci Sports Exerc 33:568–575PubMedCrossRefGoogle Scholar
  40. Ronsen O, Pedersen BK, Oritsland TR, Bahr R, Kjeldsen-Kragh J (2001b) Leukocyte counts and lymphocyte responsiveness associated with repeated bouts of strenuous endurance exercise. J Appl Physiol 91:425–434PubMedGoogle Scholar
  41. Ruy H, Jeong S-M, Jun C-D, Lee J-H, Kim J-D, Lee B-S, Chung H-T (1997) Involvement of intracellular Ca2+ during growth hormone-induced priming of human neutrophils. Brain Behav Immun 11:39–46CrossRefGoogle Scholar
  42. Schwartz NS, Clutter WE, Shah SD, Cryer PE (1987) Glycemic thresholds for activation of glucose counterregulatory systems are higher than the threshold for symptoms. J Clin Invest 79:777–781PubMedGoogle Scholar
  43. Smith JA (1997) Exercise immunology and neutrophils. Int J Sports Med 18:S46–S55PubMedCrossRefGoogle Scholar
  44. Smith JA, Gray AB, Pyne DB, Baker MS, Telford RD, Weidemann MJ (1996) Moderate exercise triggers both priming and activation of neutrophil subpopulations. Am J physiol 270:R838–R845PubMedGoogle Scholar
  45. Steensberg A, Hall G, Osada T, Sacchetti M, Saltin B, Pedersen BK (2000) Production of interleukin-6 in contracting human skeletal muscle can account for the exercise-induced increase in plasma interleukin-6. J Physiol 529:237–242PubMedCrossRefGoogle Scholar
  46. Suzuki K, Sato H, Kikuchi T, Abe T, Nakaji S, Sugawara K, Totsuka M, Sato K, Yamaya K (1996) Capacity of circulating neutrophils to produce reactive oxygen species after exhaustive exercise. J Appl Physiol 81:1213–1222PubMedGoogle Scholar
  47. Suzuki K, Totsuka M, Nakaji S, Yamada M, Kudoh S, Liu Q, Sugawara K, Yamaya K, Sato K (1999) Endurance exercise causes interaction among stress hormones, cytokines, neutrophil dynamics, and muscle damage. J Appl Physiol 87:1360–1367PubMedGoogle Scholar
  48. Tintinger GR, Theron AJ, Anderson R, Ker JA (2001) The anti-inflammatory interactions of epinephrine with human neutrophils in vitro are acheieved by cyclic AMP-mediated accelerated resequestration of cytosolic calcium. Biochem Pharmacol 61:1319–1328PubMedCrossRefGoogle Scholar
  49. Toft P, Tonnesen E, Svendsen P, Pasmussen JW (1992) Redistribution of lymphocytes after cortisol administration. APMIS 1000:154–158CrossRefGoogle Scholar
  50. Toft P, Helbo-Hansen HS, Lillevang ST, Rasmussen JW, Christensen NJ (1994) Redistribution of granulocytes during adrenaline infusion and following administration of cortisol in healthy volunteers. Acta Anaesthesiol Scand 38:254–258PubMedGoogle Scholar
  51. Walsh NP, Blannin AK, Bishop N, Robson PJ, Gleeson M (2000) Effect of oral glutamine supplementation on human neutrophil lipopolysaccharide-stimulated degranulation following prolonged exercise. Int J Sport Nutr Exerc Metab 10:39–50PubMedGoogle Scholar
  52. Wira CR, Sandoe CP, Steele MG (1990) Glucocorticoid regulation of the humoral immune system. I. In vivo effects of dexamethasone on IgA and IgG in serum and at mucosal surfaces. J Immunol 144:142–146PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  1. 1.Institute School of Sport and Exercise SciencesLoughborough UniversityLoughboroughUK
  2. 2.Department of Sports and Leisure StudiesNational Dong Hwa UniversityHualienTaiwan

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