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. 1997 Oct-Dec;32(4):344–349.

Risk of Upper Respiratory Tract Infection in Athletes: An Epidemiologic and Immunologic Perspective

David C Nieman 1
PMCID: PMC1320353  PMID: 16558471

Abstract

Objective:

The chronic and acute immune responses to both heavy and moderate exercise are reviewed, with guidelines provided for the prevention and management of upper respiratory tract infection (URTI) in athletes.

Data Sources:

Epidemiologic and experimental exercise immunology research data were used. The MEDLINE database was searched for the years 1970 to 1997 with the terms “exercise,” “immune,” “infection,” “lymphocyte,” and “neutrophil.”

Data Synthesis:

A descriptive review with summary figures and one table.

Conclusions/Recommendations:

The epidemiologic data suggest that endurance athletes are at increased risk for URTI during periods of heavy training and the 1-to 2-week period after marathon-type race events. Several researchers have reported a diminished neutrophil function in athletes during periods of intense and heavy training. Following each bout of prolonged heavy endurance exercise, several components of the immune system appear to demonstrate suppressed function for several hours. This has led to the concept of the “open window,” described as the 3- to 12-hour time period after prolonged endurance exercise when host defense is decreased and the risk of URTI is elevated. There is sufficient evidence for sports medicine professionals to encourage athletes to practice various hygienic measures to lower their risk of URTI and to avoid heavy exertion during systemic illness.

Keywords: immune system, exertion, lymphocyte, neutrophil, common cold

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Selected References

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

  1. Adams P. F., Benson V. Current estimates from the National Health Interview Survey, 1990. Vital Health Stat 10. 1991 Dec;(181):1–212. [PubMed] [Google Scholar]
  2. Ansari S. A., Springthorpe V. S., Sattar S. A., Rivard S., Rahman M. Potential role of hands in the spread of respiratory viral infections: studies with human parainfluenza virus 3 and rhinovirus 14. J Clin Microbiol. 1991 Oct;29(10):2115–2119. doi: 10.1128/jcm.29.10.2115-2119.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Baj Z., Kantorski J., Majewska E., Zeman K., Pokoca L., Fornalczyk E., Tchórzewski H., Sulowska Z., Lewicki R. Immunological status of competitive cyclists before and after the training season. Int J Sports Med. 1994 Aug;15(6):319–324. doi: 10.1055/s-2007-1021067. [DOI] [PubMed] [Google Scholar]
  4. Baslund B., Lyngberg K., Andersen V., Halkjaer Kristensen J., Hansen M., Klokker M., Pedersen B. K. Effect of 8 wk of bicycle training on the immune system of patients with rheumatoid arthritis. J Appl Physiol (1985) 1993 Oct;75(4):1691–1695. doi: 10.1152/jappl.1993.75.4.1691. [DOI] [PubMed] [Google Scholar]
  5. Behan P. O., Behan W. M., Gow J. W., Cavanagh H., Gillespie S. Enteroviruses and postviral fatigue syndrome. Ciba Found Symp. 1993;173:146–159. doi: 10.1002/9780470514382.ch9. [DOI] [PubMed] [Google Scholar]
  6. Berk L. S., Nieman D. C., Youngberg W. S., Arabatzis K., Simpson-Westerberg M., Lee J. W., Tan S. A., Eby W. C. The effect of long endurance running on natural killer cells in marathoners. Med Sci Sports Exerc. 1990 Apr;22(2):207–212. [PubMed] [Google Scholar]
  7. Brahmi Z., Thomas J. E., Park M., Park M., Dowdeswell I. R. The effect of acute exercise on natural killer-cell activity of trained and sedentary human subjects. J Clin Immunol. 1985 Sep;5(5):321–328. doi: 10.1007/BF00918251. [DOI] [PubMed] [Google Scholar]
  8. Burch G. E. Viral diseases of the heart. Acta Cardiol. 1979;34(1):5–9. [PubMed] [Google Scholar]
  9. Chandra R. K. 1990 McCollum Award lecture. Nutrition and immunity: lessons from the past and new insights into the future. Am J Clin Nutr. 1991 May;53(5):1087–1101. doi: 10.1093/ajcn/53.5.1087. [DOI] [PubMed] [Google Scholar]
  10. Chao C. C., Strgar F., Tsang M., Peterson P. K. Effects of swimming exercise on the pathogenesis of acute murine Toxoplasma gondii Me49 infection. Clin Immunol Immunopathol. 1992 Feb;62(2):220–226. doi: 10.1016/0090-1229(92)90075-y. [DOI] [PubMed] [Google Scholar]
  11. Cohen S., Tyrrell D. A., Smith A. P. Psychological stress and susceptibility to the common cold. N Engl J Med. 1991 Aug 29;325(9):606–612. doi: 10.1056/NEJM199108293250903. [DOI] [PubMed] [Google Scholar]
  12. Crary B., Borysenko M., Sutherland D. C., Kutz I., Borysenko J. Z., Benson H. Decrease in mitogen responsiveness of mononuclear cells from peripheral blood after epinephrine administration in humans. J Immunol. 1983 Feb;130(2):694–697. [PubMed] [Google Scholar]
  13. Cupps T. R., Fauci A. S. Corticosteroid-mediated immunoregulation in man. Immunol Rev. 1982;65:133–155. doi: 10.1111/j.1600-065x.1982.tb00431.x. [DOI] [PubMed] [Google Scholar]
  14. Daniels W. L., Vogel J. A., Sharp D. S., Friman G., Wright J. E., Beisel W. R., Knapik J. J. Effects of virus infection on physical performance in man. Mil Med. 1985 Jan;150(1):8–14. [PubMed] [Google Scholar]
  15. Eskola J., Ruuskanen O., Soppi E., Viljanen M. K., Järvinen M., Toivonen H., Kouvalainen K. Effect of sport stress on lymphocyte transformation and antibody formation. Clin Exp Immunol. 1978 May;32(2):339–345. [PMC free article] [PubMed] [Google Scholar]
  16. Friman G., Ilbäck N. G., Crawford D. J., Neufeld H. A. Metabolic responses to swimming exercise in Streptococcus pneumoniae infected rats. Med Sci Sports Exerc. 1991 Apr;23(4):415–421. [PubMed] [Google Scholar]
  17. Gmünder F. K., Lorenzi G., Bechler B., Joller P., Müller J., Ziegler W. H., Cogoli A. Effect of long-term physical exercise on lymphocyte reactivity: similarity to spaceflight reactions. Aviat Space Environ Med. 1988 Feb;59(2):146–151. [PubMed] [Google Scholar]
  18. Green R. L., Kaplan S. S., Rabin B. S., Stanitski C. L., Zdziarski U. Immune function in marathon runners. Ann Allergy. 1981 Aug;47(2):73–75. [PubMed] [Google Scholar]
  19. Hack V., Strobel G., Rau J. P., Weicker H. The effect of maximal exercise on the activity of neutrophil granulocytes in highly trained athletes in a moderate training period. Eur J Appl Physiol Occup Physiol. 1992;65(6):520–524. doi: 10.1007/BF00602358. [DOI] [PubMed] [Google Scholar]
  20. Hack V., Strobel G., Weiss M., Weicker H. PMN cell counts and phagocytic activity of highly trained athletes depend on training period. J Appl Physiol (1985) 1994 Oct;77(4):1731–1735. doi: 10.1152/jappl.1994.77.4.1731. [DOI] [PubMed] [Google Scholar]
  21. Hanley D. F. Medical care of the US Olympic Team. JAMA. 1976 Jul 12;236(2):147–148. [PubMed] [Google Scholar]
  22. Heath G. W., Ford E. S., Craven T. E., Macera C. A., Jackson K. L., Pate R. R. Exercise and the incidence of upper respiratory tract infections. Med Sci Sports Exerc. 1991 Feb;23(2):152–157. [PubMed] [Google Scholar]
  23. Ilbäck N. G., Friman G., Crawford D. J., Neufeld H. A. Effects of training on metabolic responses and performance capacity in Streptococcus pneumoniae infected rats. Med Sci Sports Exerc. 1991 Apr;23(4):422–427. [PubMed] [Google Scholar]
  24. Irwin M., Smith T. L., Gillin J. C. Electroencephalographic sleep and natural killer activity in depressed patients and control subjects. Psychosom Med. 1992 Jan-Feb;54(1):10–21. doi: 10.1097/00006842-199201000-00002. [DOI] [PubMed] [Google Scholar]
  25. Jokl E. The immunological status of athletes. J Sports Med Phys Fitness. 1974 Sep;14(3):165–167. [PubMed] [Google Scholar]
  26. Kokot K., Schaefer R. M., Teschner M., Gilge U., Plass R., Heidland A. Activation of leukocytes during prolonged physical exercise. Adv Exp Med Biol. 1988;240:57–63. doi: 10.1007/978-1-4613-1057-0_6. [DOI] [PubMed] [Google Scholar]
  27. Lee D. J., Meehan R. T., Robinson C., Mabry T. R., Smith M. L. Immune responsiveness and risk of illness in U.S. Air Force Academy cadets during basic cadet training. Aviat Space Environ Med. 1992 Jun;63(6):517–523. [PubMed] [Google Scholar]
  28. Lewicki R., Tchórzewski H., Denys A., Kowalska M., Golińska A. Effect of physical exercise on some parameters of immunity in conditioned sportsmen. Int J Sports Med. 1987 Oct;8(5):309–314. doi: 10.1055/s-2008-1025675. [DOI] [PubMed] [Google Scholar]
  29. MacKinnon L. T., Jenkins D. G. Decreased salivary immunoglobulins after intense interval exercise before and after training. Med Sci Sports Exerc. 1993 Jun;25(6):678–683. [PubMed] [Google Scholar]
  30. Macha M., Shlafer M., Kluger M. J. Human neutrophil hydrogen peroxide generation following physical exercise. J Sports Med Phys Fitness. 1990 Dec;30(4):412–419. [PubMed] [Google Scholar]
  31. Mackinnon L. T., Chick T. W., van As A., Tomasi T. B. The effect of exercise on secretory and natural immunity. Adv Exp Med Biol. 1987;216A:869–876. doi: 10.1007/978-1-4684-5344-7_102. [DOI] [PubMed] [Google Scholar]
  32. Mackinnon L. T., Hooper S. Mucosal (secretory) immune system responses to exercise of varying intensity and during overtraining. Int J Sports Med. 1994 Oct;15 (Suppl 3):S179–S183. doi: 10.1055/s-2007-1021134. [DOI] [PubMed] [Google Scholar]
  33. Maffulli N., Testa V., Capasso G. Post-viral fatigue syndrome. A longitudinal assessment in varsity athletes. J Sports Med Phys Fitness. 1993 Dec;33(4):392–399. [PubMed] [Google Scholar]
  34. Müns G. Effect of long-distance running on polymorphonuclear neutrophil phagocytic function of the upper airways. Int J Sports Med. 1994 Feb;15(2):96–99. doi: 10.1055/s-2007-1021027. [DOI] [PubMed] [Google Scholar]
  35. 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]
  36. 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]
  37. Nieman D. C., Brendle D., Henson D. A., Suttles J., Cook V. D., Warren B. J., Butterworth D. E., Fagoaga O. R., Nehlsen-Cannarella S. L. Immune function in athletes versus nonathletes. Int J Sports Med. 1995 Jul;16(5):329–333. doi: 10.1055/s-2007-973014. [DOI] [PubMed] [Google Scholar]
  38. Nieman D. C., Buckley K. S., Henson D. A., Warren B. J., Suttles J., Ahle J. C., Simandle S., Fagoaga O. R., Nehlsen-Cannarella S. L. Immune function in marathon runners versus sedentary controls. Med Sci Sports Exerc. 1995 Jul;27(7):986–992. doi: 10.1249/00005768-199507000-00006. [DOI] [PubMed] [Google Scholar]
  39. Nieman D. C., Cook V. D., Henson D. A., Suttles J., Rejeski W. J., Ribisl P. M., Fagoaga O. R., Nehlsen-Cannarella S. L. Moderate exercise training and natural killer cell cytotoxic activity in breast cancer patients. Int J Sports Med. 1995 Jul;16(5):334–337. doi: 10.1055/s-2007-973015. [DOI] [PubMed] [Google Scholar]
  40. Nieman D. C. Exercise, infection, and immunity. Int J Sports Med. 1994 Oct;15 (Suppl 3):S131–S141. doi: 10.1055/s-2007-1021128. [DOI] [PubMed] [Google Scholar]
  41. Nieman D. C., Fagoaga O. R., Butterworth D. E., Warren B. J., Utter A., Davis J. M., Henson D. A., Nehlsen-Cannarella S. L. Carbohydrate supplementation affects blood granulocyte and monocyte trafficking but not function after 2.5 h or running. Am J Clin Nutr. 1997 Jul;66(1):153–159. doi: 10.1093/ajcn/66.1.153. [DOI] [PubMed] [Google Scholar]
  42. Nieman D. C., Henson D. A., Gusewitch G., Warren B. J., Dotson R. C., Butterworth D. E., Nehlsen-Cannarella S. L. Physical activity and immune function in elderly women. Med Sci Sports Exerc. 1993 Jul;25(7):823–831. doi: 10.1249/00005768-199307000-00011. [DOI] [PubMed] [Google Scholar]
  43. Nieman D. C., Johanssen L. M., Lee J. W., Arabatzis K. Infectious episodes in runners before and after the Los Angeles Marathon. J Sports Med Phys Fitness. 1990 Sep;30(3):316–328. [PubMed] [Google Scholar]
  44. Nieman D. C., Johanssen L. M., Lee J. W. Infectious episodes in runners before and after a roadrace. J Sports Med Phys Fitness. 1989 Sep;29(3):289–296. [PubMed] [Google Scholar]
  45. Nieman D. C., Miller A. R., Henson D. A., Warren B. J., Gusewitch G., Johnson R. L., Davis J. M., Butterworth D. E., Herring J. L., Nehlsen-Cannarella S. L. Effect of high- versus moderate-intensity exercise on lymphocyte subpopulations and proliferative response. Int J Sports Med. 1994 May;15(4):199–206. doi: 10.1055/s-2007-1021047. [DOI] [PubMed] [Google Scholar]
  46. 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]
  47. Nieman D. C., Nehlsen-Cannarella S. L., Markoff P. A., Balk-Lamberton A. J., Yang H., Chritton D. B., Lee J. W., Arabatzis K. The effects of moderate exercise training on natural killer cells and acute upper respiratory tract infections. Int J Sports Med. 1990 Dec;11(6):467–473. doi: 10.1055/s-2007-1024839. [DOI] [PubMed] [Google Scholar]
  48. Nieman D. C., Simandle S., Henson D. A., Warren B. J., Suttles J., Davis J. M., Buckley K. S., Ahle J. C., Butterworth D. E., Fagoaga O. R. Lymphocyte proliferative response to 2.5 hours of running. Int J Sports Med. 1995 Aug;16(6):404–409. doi: 10.1055/s-2007-973028. [DOI] [PubMed] [Google Scholar]
  49. Oshida Y., Yamanouchi K., Hayamizu S., Sato Y. Effect of acute physical exercise on lymphocyte subpopulations in trained and untrained subjects. Int J Sports Med. 1988 Apr;9(2):137–140. doi: 10.1055/s-2007-1024995. [DOI] [PubMed] [Google Scholar]
  50. Oshida Y., Yamanouchi K., Hayamizu S., Sato Y. Effect of acute physical exercise on lymphocyte subpopulations in trained and untrained subjects. Int J Sports Med. 1988 Apr;9(2):137–140. doi: 10.1055/s-2007-1024995. [DOI] [PubMed] [Google Scholar]
  51. Papa S., Vitale M., Mazzotti G., Neri L. M., Monti G., Manzoli F. A. Impaired lymphocyte stimulation induced by long-term training. Immunol Lett. 1989 Jul;22(1):29–33. doi: 10.1016/0165-2478(89)90138-7. [DOI] [PubMed] [Google Scholar]
  52. Pedersen B. K., Tvede N., Christensen L. D., Klarlund K., Kragbak S., Halkjr-Kristensen J. Natural killer cell activity in peripheral blood of highly trained and untrained persons. Int J Sports Med. 1989 Apr;10(2):129–131. doi: 10.1055/s-2007-1024888. [DOI] [PubMed] [Google Scholar]
  53. 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]
  54. 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]
  55. Peters E. M., Bateman E. D. Ultramarathon running and upper respiratory tract infections. An epidemiological survey. S Afr Med J. 1983 Oct 1;64(15):582–584. [PubMed] [Google Scholar]
  56. Peters E. M., Goetzsche J. M., Grobbelaar B., Noakes T. D. Vitamin C supplementation reduces the incidence of postrace symptoms of upper-respiratory-tract infection in ultramarathon runners. Am J Clin Nutr. 1993 Feb;57(2):170–174. doi: 10.1093/ajcn/57.2.170. [DOI] [PubMed] [Google Scholar]
  57. Pyne D. B., Baker M. S., Fricker P. A., McDonald W. A., Telford R. D., Weidemann M. J. Effects of an intensive 12-wk training program by elite swimmers on neutrophil oxidative activity. Med Sci Sports Exerc. 1995 Apr;27(4):536–542. [PubMed] [Google Scholar]
  58. Pyne D. B. Regulation of neutrophil function during exercise. Sports Med. 1994 Apr;17(4):245–258. doi: 10.2165/00007256-199417040-00005. [DOI] [PubMed] [Google Scholar]
  59. Roberts J. A. Loss of form in young athletes due to viral infection. Br Med J (Clin Res Ed) 1985 Feb 2;290(6465):357–358. doi: 10.1136/bmj.290.6465.357. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Roberts J. A. Viral illnesses and sports performance. Sports Med. 1986 Jul-Aug;3(4):298–303. doi: 10.2165/00007256-198603040-00006. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Sharp J. C. Viruses and the athlete. Br J Sports Med. 1989 Mar;23(1):47–48. doi: 10.1136/bjsm.23.1.47. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Shephard R. J., Kavanagh T., Mertens D. J., Qureshi S., Clark M. Personal health benefits of Masters athletics competition. Br J Sports Med. 1995 Mar;29(1):35–40. doi: 10.1136/bjsm.29.1.35. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Shinkai S., Kohno H., Kimura K., Komura T., Asai H., Inai R., Oka K., Kurokawa Y., Shephard R. Physical activity and immune senescence in men. Med Sci Sports Exerc. 1995 Nov;27(11):1516–1526. [PubMed] [Google Scholar]
  64. Shinkai S., Kurokawa Y., Hino S., Hirose M., Torii J., Watanabe S., Watanabe S., Shiraishi S., Oka K., Watanabe T. Triathlon competition induced a transient immunosuppressive change in the peripheral blood of athletes. J Sports Med Phys Fitness. 1993 Mar;33(1):70–78. [PubMed] [Google Scholar]
  65. Shinkai S., Shore S., Shek P. N., Shephard R. J. Acute exercise and immune function. Relationship between lymphocyte activity and changes in subset counts. Int J Sports Med. 1992 Aug;13(6):452–461. doi: 10.1055/s-2007-1021297. [DOI] [PubMed] [Google Scholar]
  66. Smith J. A., Telford R. D., Mason I. B., Weidemann M. J. Exercise, training and neutrophil microbicidal activity. Int J Sports Med. 1990 Jun;11(3):179–187. doi: 10.1055/s-2007-1024788. [DOI] [PubMed] [Google Scholar]
  67. Tomasi T. B., Trudeau F. B., Czerwinski D., Erredge S. Immune parameters in athletes before and after strenuous exercise. J Clin Immunol. 1982 Jul;2(3):173–178. doi: 10.1007/BF00915219. [DOI] [PubMed] [Google Scholar]

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