Skip to main content
PMC home page
British Journal of Sports Medicine logoLink to British Journal of Sports Medicine
. 2005 Mar;39(3):171–177. doi: 10.1136/bjsm.2004.013060

Does prolonged cycling of moderate intensity affect immune cell function?

J Scharhag 1, T Meyer 1, H Gabriel 1, B Schlick 1, O Faude 1, W Kindermann 1, R Shephard 1
PMCID: PMC1725141  PMID: 15728699

Abstract

Background: Prolonged exercise may induce temporary immunosuppression with a presumed increased susceptibility for infection. However, there are only few data on immune cell function after prolonged cycling at moderate intensities typical for road cycling training sessions.

Methods: The present study examined the influence on immune cell function of 4 h of cycling at a constant intensity of 70% of the individual anaerobic threshold. Interleukin-6 (IL-6) and C-reactive protein (CRP), leukocyte and lymphocyte populations, activities of natural killer (NK), neutrophils, and monocytes were examined before and after exercise, and also on a control day without exercise.

Results: Cycling for 4 h induced a moderate acute phase response with increases in IL-6 from 1.0 (SD 0.5) before to 9.6 (5.6) pg/ml 1 h after exercise and CRP from 0.5 (SD 0.4) before to 1.8 (1.3) mg/l 1 day after exercise. Although absolute numbers of circulating NK cells, monocytes, and neutrophils increased during exercise, on a per cell basis NK cell activity, neutrophil and monocyte phagocytosis, and monocyte oxidative burst did not significantly change after exercise. However, a minor effect over time for neutrophil oxidative burst was noted, tending to decrease after exercise.

Conclusions: Prolonged cycling at moderate intensities does not seem to seriously alter the function of cells of the first line of defence. Therefore, the influence of a single typical road cycling training session on the immune system is only moderate and appears to be safe from an immunological point of view.

Full Text

The Full Text of this article is available as a PDF (111.3 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Castell L. M., Poortmans J. R., Leclercq R., Brasseur M., Duchateau J., Newsholme E. A. Some aspects of the acute phase response after a marathon race, and the effects of glutamine supplementation. Eur J Appl Physiol Occup Physiol. 1997;75(1):47–53. doi: 10.1007/s004210050125. [DOI] [PubMed] [Google Scholar]
  2. Da Prada M., Zürcher Simultaneous radioenzymatic determination of plasma and tissue adrenaline, noradrenaline and dopamine within the femtomole range. Life Sci. 1976 Oct 15;19(8):1161–1174. doi: 10.1016/0024-3205(76)90251-4. [DOI] [PubMed] [Google Scholar]
  3. Dill D. B., Costill D. L. Calculation of percentage changes in volumes of blood, plasma, and red cells in dehydration. J Appl Physiol. 1974 Aug;37(2):247–248. doi: 10.1152/jappl.1974.37.2.247. [DOI] [PubMed] [Google Scholar]
  4. Febbraio Mark A., Steensberg Adam, Keller Charlotte, Starkie Rebecca L., Nielsen Henning B., Krustrup Peter, Ott Peter, Secher Niels H., Pedersen Bente K. Glucose ingestion attenuates interleukin-6 release from contracting skeletal muscle in humans. J Physiol. 2003 Apr 17;549(Pt 2):607–612. doi: 10.1113/jphysiol.2003.042374. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Ferrandez M. D., De la Fuente M. Effects of age, sex and physical exercise on the phagocytic process of murine peritoneal macrophages. Acta Physiol Scand. 1999 May;166(1):47–53. doi: 10.1046/j.1365-201x.1999.00535.x. [DOI] [PubMed] [Google Scholar]
  6. Gabriel H., Müller H. J., Kettler K., Brechtel L., Urhausen A., Kindermann W. Increased phagocytic capacity of the blood, but decreased phagocytic activity per individual circulating neutrophil after an ultradistance run. Eur J Appl Physiol Occup Physiol. 1995;71(2-3):281–284. doi: 10.1007/BF00854992. [DOI] [PubMed] [Google Scholar]
  7. Gabriel H., Müller H. J., Urhausen A., Kindermann W. Suppressed PMA-induced oxidative burst and unimpaired phagocytosis of circulating granulocytes one week after a long endurance exercise. Int J Sports Med. 1994 Oct;15(7):441–445. doi: 10.1055/s-2007-1021085. [DOI] [PubMed] [Google Scholar]
  8. Gannon G. A., Rhind S. G., Suzui M., Shek P. N., Shephard R. J. Circulating levels of peripheral blood leucocytes and cytokines following competitive cycling. Can J Appl Physiol. 1997 Apr;22(2):133–147. doi: 10.1139/h97-011. [DOI] [PubMed] [Google Scholar]
  9. Gannon G. A., Rhind S. G., Suzui M., Shek P. N., Shephard R. J. Circulating levels of peripheral blood leucocytes and cytokines following competitive cycling. Can J Appl Physiol. 1997 Apr;22(2):133–147. doi: 10.1139/h97-011. [DOI] [PubMed] [Google Scholar]
  10. Hiscock N., Petersen E. W., Krzywkowski K., Boza J., Halkjaer-Kristensen J., Pedersen B. K. Glutamine supplementation further enhances exercise-induced plasma IL-6. J Appl Physiol (1985) 2003 Feb 28;95(1):145–148. doi: 10.1152/japplphysiol.00471.2002. [DOI] [PubMed] [Google Scholar]
  11. Keller Charlotte, Keller Pernille, Marshal Sonya, Pedersen Bente Klarlund. IL-6 gene expression in human adipose tissue in response to exercise--effect of carbohydrate ingestion. J Physiol. 2003 Jun 6;550(Pt 3):927–931. doi: 10.1113/jphysiol.2003.044883. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Krause R., Patruta S., Daxböck F., Fladerer P., Biegelmayer C., Wenisch C. Effect of vitamin C on neutrophil function after high-intensity exercise. Eur J Clin Invest. 2001 Mar;31(3):258–263. doi: 10.1046/j.1365-2362.2001.00797.x. [DOI] [PubMed] [Google Scholar]
  13. Lucia A., Hoyos J., Chicharro J. L. Physiology of professional road cycling. Sports Med. 2001;31(5):325–337. doi: 10.2165/00007256-200131050-00004. [DOI] [PubMed] [Google Scholar]
  14. Malpica M. I., Rodríguez A. B., Sáez M. C., García J. J., Barriga C., Ortega E. In-vitro study of the effect of adrenaline on the functional capacity of human neutrophils: role during exercise. J Neuroendocrinol. 2002 Oct;14(10):824–828. doi: 10.1046/j.1365-2826.2002.00847.x. [DOI] [PubMed] [Google Scholar]
  15. McFarlin Brian K., Mitchell Joel B., McFarlin Meredith A., Steinhoff Gina M. Repeated endurance exercise affects leukocyte number but not NK cell activity. Med Sci Sports Exerc. 2003 Jul;35(7):1130–1138. doi: 10.1249/01.MSS.0000074463.36752.87. [DOI] [PubMed] [Google Scholar]
  16. Meyer T., Gabriel H. H., Kindermann W. Is determination of exercise intensities as percentages of VO2max or HRmax adequate? Med Sci Sports Exerc. 1999 Sep;31(9):1342–1345. doi: 10.1097/00005768-199909000-00017. [DOI] [PubMed] [Google Scholar]
  17. Meyer T., Gabriel H. H., Rätz M., Müller H. J., Kindermann W. Anaerobic exercise induces moderate acute phase response. Med Sci Sports Exerc. 2001 Apr;33(4):549–555. doi: 10.1097/00005768-200104000-00007. [DOI] [PubMed] [Google Scholar]
  18. Middleton Derek, Curran Martin, Maxwell Lynne. Natural killer cells and their receptors. Transpl Immunol. 2002 Aug;10(2-3):147–164. doi: 10.1016/s0966-3274(02)00062-x. [DOI] [PubMed] [Google Scholar]
  19. Miles M. P., Mackinnon L. T., Grove D. S., Williams N. I., Bush J. A., Marx J. O., Kraemer W. J., Mastro A. M. The relationship of natural killer cell counts, perforin mRNA and CD2 expression to post-exercise natural killer cell activity in humans. Acta Physiol Scand. 2002 Apr;174(4):317–325. doi: 10.1046/j.1365-201x.2002.00958.x. [DOI] [PubMed] [Google Scholar]
  20. Moldoveanu A. I., Shephard R. J., Shek P. N. Exercise elevates plasma levels but not gene expression of IL-1beta, IL-6, and TNF-alpha in blood mononuclear cells. J Appl Physiol (1985) 2000 Oct;89(4):1499–1504. doi: 10.1152/jappl.2000.89.4.1499. [DOI] [PubMed] [Google Scholar]
  21. Nagao F., Suzui M., Takeda K., Yagita H., Okumura K. Mobilization of NK cells by exercise: downmodulation of adhesion molecules on NK cells by catecholamines. Am J Physiol Regul Integr Comp Physiol. 2000 Oct;279(4):R1251–R1256. doi: 10.1152/ajpregu.2000.279.4.R1251. [DOI] [PubMed] [Google Scholar]
  22. Nehlsen-Cannarella S. L., Fagoaga O. R., Nieman D. C., Henson D. A., Butterworth D. E., Schmitt R. L., Bailey E. M., Warren B. J., Utter A., Davis J. M. Carbohydrate and the cytokine response to 2.5 h of running. J Appl Physiol (1985) 1997 May;82(5):1662–1667. doi: 10.1152/jappl.1997.82.5.1662. [DOI] [PubMed] [Google Scholar]
  23. Nieman D. C., Ahle J. C., Henson D. A., Warren B. J., Suttles J., Davis J. M., Buckley K. S., Simandle S., Butterworth D. E., Fagoaga O. R. Indomethacin does not alter natural killer cell response to 2.5 h of running. J Appl Physiol (1985) 1995 Sep;79(3):748–755. doi: 10.1152/jappl.1995.79.3.748. [DOI] [PubMed] [Google Scholar]
  24. Nieman D. C., Davis J. M., Henson D. A., Walberg-Rankin J., Shute M., Dumke C. L., Utter A. C., Vinci D. M., Carson J. A., Brown A. Carbohydrate ingestion influences skeletal muscle cytokine mRNA and plasma cytokine levels after a 3-h run. J Appl Physiol (1985) 2003 Jan 17;94(5):1917–1925. doi: 10.1152/japplphysiol.01130.2002. [DOI] [PubMed] [Google Scholar]
  25. Nieman D. C., Miller A. R., Henson D. A., Warren B. J., Gusewitch G., Johnson R. L., Davis J. M., Butterworth D. E., Nehlsen-Cannarella S. L. Effects of high- vs moderate-intensity exercise on natural killer cell activity. Med Sci Sports Exerc. 1993 Oct;25(10):1126–1134. [PubMed] [Google Scholar]
  26. Nieman D. C., Nehlsen-Cannarella S. L., Fagoaga O. R., Henson D. A., Utter A., Davis J. M., Williams F., Butterworth D. E. Effects of mode and carbohydrate on the granulocyte and monocyte response to intensive, prolonged exercise. J Appl Physiol (1985) 1998 Apr;84(4):1252–1259. doi: 10.1152/jappl.1998.84.4.1252. [DOI] [PubMed] [Google Scholar]
  27. Nieman D. C., Nehlsen-Cannarella S. L., Fagoaga O. R., Henson D. A., Utter A., Davis J. M., Williams F., Butterworth D. E. Influence of mode and carbohydrate on the cytokine response to heavy exertion. Med Sci Sports Exerc. 1998 May;30(5):671–678. doi: 10.1097/00005768-199805000-00005. [DOI] [PubMed] [Google Scholar]
  28. Nieman D. C. Nutrition, exercise, and immune system function. Clin Sports Med. 1999 Jul;18(3):537–548. doi: 10.1016/s0278-5919(05)70167-8. [DOI] [PubMed] [Google Scholar]
  29. Ostrowski K., Rohde T., Asp S., Schjerling P., Pedersen B. K. Pro- and anti-inflammatory cytokine balance in strenuous exercise in humans. J Physiol. 1999 Feb 15;515(Pt 1):287–291. doi: 10.1111/j.1469-7793.1999.287ad.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Peake Jonathan M. Exercise-induced alterations in neutrophil degranulation and respiratory burst activity: possible mechanisms of action. Exerc Immunol Rev. 2002;8:49–100. [PubMed] [Google Scholar]
  31. Pedersen B. K., Tvede N., Klarlund K., Christensen L. D., Hansen F. R., Galbo H., Kharazmi A., Halkjaer-Kristensen J. Indomethacin in vitro and in vivo abolishes post-exercise suppression of natural killer cell activity in peripheral blood. Int J Sports Med. 1990 Apr;11(2):127–131. doi: 10.1055/s-2007-1024776. [DOI] [PubMed] [Google Scholar]
  32. Pedersen B. K., Ullum H. NK cell response to physical activity: possible mechanisms of action. Med Sci Sports Exerc. 1994 Feb;26(2):140–146. doi: 10.1249/00005768-199402000-00003. [DOI] [PubMed] [Google Scholar]
  33. Pedersen Bente Klarlund, Steensberg Adam, Keller Pernille, Keller Charlotte, Fischer Christian, Hiscock Natalie, van Hall Gerrit, Plomgaard Peter, Febbraio Mark A. Muscle-derived interleukin-6: lipolytic, anti-inflammatory and immune regulatory effects. Pflugers Arch. 2003 Feb 18;446(1):9–16. doi: 10.1007/s00424-002-0981-z. [DOI] [PubMed] [Google Scholar]
  34. Pyne D. B., Baker M. S., Smith J. A., Telford R. D., Weidemann M. J. Exercise and the neutrophil oxidative burst: biological and experimental variability. Eur J Appl Physiol Occup Physiol. 1996;74(6):564–571. doi: 10.1007/BF02376774. [DOI] [PubMed] [Google Scholar]
  35. Rowbottom D. G., Green K. J. Acute exercise effects on the immune system. Med Sci Sports Exerc. 2000 Jul;32(7 Suppl):S396–S405. doi: 10.1097/00005768-200007001-00004. [DOI] [PubMed] [Google Scholar]
  36. Scharhag J., Meyer T., Gabriel H. H. W., Auracher M., Kindermann W. Mobilization and oxidative burst of neutrophils are influenced by carbohydrate supplementation during prolonged cycling in humans. Eur J Appl Physiol. 2002 Jul 24;87(6):584–587. doi: 10.1007/s00421-002-0642-0. [DOI] [PubMed] [Google Scholar]
  37. Shephard R. J. Special feature for the Olympics: effects of exercise on the immune system: overview of the epidemiology of exercise immunology. Immunol Cell Biol. 2000 Oct;78(5):485–495. doi: 10.1111/j.1440-1711.2000.t01-1-.x. [DOI] [PubMed] [Google Scholar]
  38. Starkie R. L., Rolland J., Angus D. J., Anderson M. J., Febbraio M. A. Circulating monocytes are not the source of elevations in plasma IL-6 and TNF-alpha levels after prolonged running. Am J Physiol Cell Physiol. 2001 Apr;280(4):C769–C774. doi: 10.1152/ajpcell.2001.280.4.C769. [DOI] [PubMed] [Google Scholar]
  39. Steensberg A., Toft A. D., Bruunsgaard H., Sandmand M., Halkjaer-Kristensen J., Pedersen B. K. Strenuous exercise decreases the percentage of type 1 T cells in the circulation. J Appl Physiol (1985) 2001 Oct;91(4):1708–1712. doi: 10.1152/jappl.2001.91.4.1708. [DOI] [PubMed] [Google Scholar]
  40. Steensberg A., van Hall G., Osada T., Sacchetti M., Saltin B., Klarlund Pedersen B. Production of interleukin-6 in contracting human skeletal muscles can account for the exercise-induced increase in plasma interleukin-6. J Physiol. 2000 Nov 15;529(Pt 1):237–242. doi: 10.1111/j.1469-7793.2000.00237.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Steensberg Adam, Fischer Christian P., Keller Charlotte, Møller Kirsten, Pedersen Bente Klarlund. IL-6 enhances plasma IL-1ra, IL-10, and cortisol in humans. Am J Physiol Endocrinol Metab. 2003 Aug;285(2):E433–E437. doi: 10.1152/ajpendo.00074.2003. [DOI] [PubMed] [Google Scholar]
  42. Stegmann H., Kindermann W., Schnabel A. Lactate kinetics and individual anaerobic threshold. Int J Sports Med. 1981 Aug;2(3):160–165. doi: 10.1055/s-2008-1034604. [DOI] [PubMed] [Google Scholar]
  43. Suwa T., Hogg J. C., English D., Van Eeden S. F. Interleukin-6 induces demargination of intravascular neutrophils and shortens their transit in marrow. Am J Physiol Heart Circ Physiol. 2000 Dec;279(6):H2954–H2960. doi: 10.1152/ajpheart.2000.279.6.H2954. [DOI] [PubMed] [Google Scholar]
  44. Suzuki Katsuhiko, Nakaji Shigeyuki, Yamada Mutsuo, Liu Qiang, Kurakake Shigeyoshi, Okamura Noriyoshi, Kumae Takashi, Umeda Takashi, Sugawara Kazuo. Impact of a competitive marathon race on systemic cytokine and neutrophil responses. Med Sci Sports Exerc. 2003 Feb;35(2):348–355. doi: 10.1249/01.MSS.0000048861.57899.04. [DOI] [PubMed] [Google Scholar]
  45. Suzuki Katsuhiko, Nakaji Shigeyuki, Yamada Mutsuo, Totsuka Manabu, Sato Koki, Sugawara Kazuo. Systemic inflammatory response to exhaustive exercise. Cytokine kinetics. Exerc Immunol Rev. 2002;8:6–48. [PubMed] [Google Scholar]
  46. Taylor C., Rogers G., Goodman C., Baynes R. D., Bothwell T. H., Bezwoda W. R., Kramer F., Hattingh J. Hematologic, iron-related, and acute-phase protein responses to sustained strenuous exercise. J Appl Physiol (1985) 1987 Feb;62(2):464–469. doi: 10.1152/jappl.1987.62.2.464. [DOI] [PubMed] [Google Scholar]

Articles from British Journal of Sports Medicine are provided here courtesy of BMJ Publishing Group

RESOURCES