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Ultra Marathon Race Competition and Immune Function

  • David C. NiemanEmail author
Chapter
Part of the Heat Shock Proteins book series (HESP, volume 5)

Abstract

This chapter reviews key exercise immunology findings from five years of research on 350 athletes in the 160-km Western States Endurance Run (WSER), a point-to-point trail run in the Sierra Nevada Mountains of northern California. Until this series of studies on WSER ultra-marathoners, little was known regarding the response of the immune system to severe exertion. This chapter describes how the immune system responds to running 160 km and underlying mechanisms including oxidative stress, muscle damage, inflammation, endotoxemia, and ibuprofen use

Keywords:

Cytokines running immune function ibuprofen oxidative stress inflammation neutrophils 

Abbreviations

ALT

alanine aminotransferase

AST

asparate aminotransferase

BMI

body mass index

BUN

blood urea nitrogen

CK

creatine kinase

CRP

C-reactive protein

DOMS

delayed onset of muscle soreness

G-CSF

granulocyte colony-stimulating factor

IgA

immunoglobulin A

IL-6

interleukin-6

LPS

lipopolysaccharide

MCP-1

monocyte chemoattractant protein 1

MIF

macrophage migration inhibitory factor

MIP-1β

macrophage inflammatory protein 1 beta

NK

natural killer

NSAIDS

Non-steroidal anti-inflammatory drugs

RPE

ratings of perceived exertion

TNF-α

tumor necrosis factor-alpha

URTI

upper respiratory tract infections

WSER

Western States Endurance Run

References

  1. Akerström, T.C. and Pedersen, B.K. (2007). Strategies to enhance immune function for marathon runners: what can be done? Sports Med. 37, 416–419.CrossRefPubMedGoogle Scholar
  2. Bosenberg, A.T., Brock-Utne, J.G., Gaffin, S.L., Wells, M.T., and Blake, G.T. (1988). Strenuous exercise causes systemic endotoxemia. J. Appl. Physiol. 65, 106–108.PubMedGoogle Scholar
  3. Brock-Utne, J.G., Gaffin, S.L., Wells, M.T. et al. (1988). Endotoxemia in exhausted runners after a long-distance race. S. Afr. Med. J. 73, 533–536.PubMedGoogle Scholar
  4. Bruunsgaard, H., Galbo, H., Halkjaer-Kristensen, J., Johansen, T.L., MacLean, D.A., and Pedersen, B.K. (1997). Exercise-induced increase in serum interleukin-6 in humans is related to muscle damage. J. Physiol. 499(Pt 3), 833–841.PubMedGoogle Scholar
  5. Bruunsgaard, H., Hartkopp, A., Mohr, T. et al. (1997). In vivo cell-mediated immunity and vaccination response following prolonged, intense exercise. Med. Sci. Sports Exerc. 29, 1176–1181.PubMedGoogle Scholar
  6. Camus, G., Poortmans, J., Nys, M. et al. (1997). Mild endotoxemia and the inflammatory response induced by a marathon race. Clin. Sci. (Lond.) 92, 415–422.Google Scholar
  7. Camus, G., Nys, M., Poortmans, J.R. et al. (1998). Endotoxemia, production of tumor necrosis factor alpha and polymorphonuclear neutrophil activation following strenuous exercise in humans. Eur. J. Appl. Physiol. 79, 62–68.CrossRefGoogle Scholar
  8. Donnelly, A.E., Maughan, R.J., and Whiting, P.H. (1990). Effects of ibuprofen on exercise-induced muscle soreness and indices of muscle damage. Br. J. Sports Med. 24, 191–195.CrossRefPubMedGoogle Scholar
  9. Dumke, C.L., Nieman, D.C., Oley, K., and Lind, R.H. (2007). Ibuprofen does not effect serum electrolytes following an ultradistance run. Br. J. Sports Med. 41, 492–496.CrossRefPubMedGoogle Scholar
  10. Farquhar, W.B., Morgan, A.L., Zambraski, E.J., and Kenney, W.L. (1999). Effect of acetaminophen and ibuprofen on renal function in the stressed kidney. J. Appl. Physiol. 86, 598–604.PubMedGoogle Scholar
  11. Frydelund-Larsen, L., Penkowa, M., Akerstrom, T., Zankari, A., Nielsen, S., and Pedersen, B.K. (2007). Exercise induces interleukin-8 receptor (CXCR2) expression in human skeletal muscle. Exp. Physiol. 92, 233–240.CrossRefPubMedGoogle Scholar
  12. Gleeson, M. (2006). Immune system adaptation in elite athletes. Curr. Opin. Clin. Nutr. Metab. Care 9, 659–665.CrossRefPubMedGoogle Scholar
  13. Gleeson, M., McDonald, W.A., Pyne, D.B. et al. (1999). Salivary IgA levels and infection risk in elite swimmers. Med. Sci. Sports Exerc. 31, 67–73.CrossRefPubMedGoogle Scholar
  14. Gleeson, M., McDonald, W.A., Pyne, D.B. et al. (2000). Immune status and respiratory illness for elite swimmers during a 12-week training cycle. Int. J. Sports Med. 21, 302–307.CrossRefPubMedGoogle Scholar
  15. Gleeson, M. and Pyne, D.B. (2000). Special feature for the Olympics: effects of exercise on the immune system: exercise effects on mucosal immunity. Immunol. Cell. Biol. 78, 536–544.CrossRefPubMedGoogle Scholar
  16. Henson, D.A., Nieman, D.C., Davis, J.M. et al. (2008). Post-160-km race illness rates and decreases in granulocyte oxidative burst activity and salivary IgA output are not countered by quercetin ingestion. Int. J. Sports Med. 29, 856–863.CrossRefPubMedGoogle Scholar
  17. Jeukendrup, A.E., Vet-Joop, K., Sturk, A. et al. (2000). Relationship between gastro-intestinal complaints and endotoxemia, cytokine release and the acute-phase reaction during and after a long-distance triathlon in highly trained men. Clin. Sci. 98, 47–55.CrossRefPubMedGoogle Scholar
  18. Keller, C., Steensberg, A., Pilegaard, H. et al. (2001). Transcriptional activation of the IL-6 gene in human contracting skeletal muscle: influence of muscle glycogen content. FASEB J. 15, 2748–2750.PubMedGoogle Scholar
  19. Kim, H.J., Lee, Y.H., and Kim, C.K. (2007). Biomarkers of muscle and cartilage damage and inflammation during a 200 km run. Eur. J. Appl. Physiol. 99, 443–447.CrossRefPubMedGoogle Scholar
  20. Krzywkowski, K., Petersen, E.W., Ostrowski, K. et al. (2001). Effect of glutamine and protein supplementation on exercise-induced decreases in salivary IgA. J. Appl. Physiol. 91, 832–838.PubMedGoogle Scholar
  21. Lambert, G.P. (2004). Role of gastrointestinal permeability in exertional heatstroke. Exerc. Sport Sci. Rev. 32, 185–190.CrossRefPubMedGoogle Scholar
  22. Lambert, G.P., Broussard, L.J., Mason, B.L., Mauermann, W.J., and Gisolfi, C.V. (2001). Gastrointestinal permeability during exercise, effects of aspirin and energy-containing beverages. J. Appl. Physiol. 90, 2075–2080.PubMedGoogle Scholar
  23. Lehtonen, O.P., Tenovuo, J., Aaltonen, A.S., and Vilja, P. (1987). Immunoglobulins and innate factors of immunity in saliva of children prone to respiratory infections. Acta. Pathol. Microbiol. Immunol. Scand. 95, 34–40.Google Scholar
  24. McAnulty, S.R., McAnulty, L.S., Nieman, D.C., Morrow, J.D., Dumke, C.L., and Henson, D.A. (2007a). Effect of NSAID on muscle injury and oxidative stress. Int. J. Sports Med. 28, 909–915.CrossRefPubMedGoogle Scholar
  25. McAnulty, S.R., Owens, J.T., McAnulty, L.S. et al. (2007b). Ibuprofen use during extreme exercise: effects on oxidative stress and PGE2. Med. Sci. Sports Exerc. 39, 1075–1079.CrossRefPubMedGoogle Scholar
  26. Nielsen, H.G. and Lyberg, T. (2004). Long-distance running modulates the expression of leucocyte and endothelial adhesion molecules. Scand. J. Immunol. 60, 356–362.CrossRefPubMedGoogle Scholar
  27. Nielsen, S. and Pedersen, B.K. (2008). Skeletal muscle as an immunogenic organ. Curr. Opin. Pharmacol. 8, 346–351.CrossRefPubMedGoogle Scholar
  28. Nieman, D.C. (2000a). Exercise effects on systemic immunity. Immunol. Cell Biol. 78, 496–501.Google Scholar
  29. Nieman, D.C. (2000b). Is infection risk linked to exercise workload? Med. Sci. Sports Exerc. 32(suppl 7), S406–S411.PubMedGoogle Scholar
  30. Nieman, D.C. (2007). Marathon training and immune function. Sports Med. 37, 412–415.CrossRefPubMedGoogle Scholar
  31. Nieman, D.C., Davis, J.M., Henson, D.A. et al. (2003a). Carbohydrate ingestion influences skeletal muscle cytokine mRNA and plasma cytokine levels after a 3-h run. J. Appl. Physiol. 94, 1917–1925.PubMedGoogle Scholar
  32. Nieman, D.C., Dumke, C.L., Henson, D.A., McAnulty, S.R., Gross, S.J., and Lind, R.L. (2005). Muscle damage is linked to cytokine changes following a 160-km race. Brain Beh. Immun. 19, 398–403.CrossRefGoogle Scholar
  33. Nieman, D.C., Dumke, C.L., Henson, D.A. et al. (2003b). Immune and oxidative changes during and following the Western States Endurance Run. Int. J. Sports Med. 24, 541–547.CrossRefPubMedGoogle Scholar
  34. Nieman, D.C., Henson, D.A., Davis, J.M. et al. (2006a). Blood leukocyte mRNA expression for IL-10, IL-1ra, and IL-8, but not IL-6, increases after exercise. J. Interferon Cytokine Res. 26, 668–674.CrossRefPubMedGoogle Scholar
  35. Nieman, D.C., Henson, D.A., Davis, J.M. et al. (2007). Quercetin ingestion does not alter cytokine changes in athletes competing in the Western States Endurance Run. J. Interferon Cytokine Res. 27, 1003–1012.CrossRefPubMedGoogle Scholar
  36. Nieman, D.C., Henson, D.A., Dumke, D.L., Lind, R.H., Shooter, L.R., and Gross, S.J. (2006b). Relationship between salivary IgA secretion and upper respiratory tract infection following a 160-km race. J. Sports Med. Phys. Fit. 46, 158–162.Google Scholar
  37. Nieman, D.C., Henson, D.A., Fagoaga, O.R. et al. (2002a). Change in salivary IgA following a competitive marathon race. Int. J. Sports Med. 23, 69–75.CrossRefPubMedGoogle Scholar
  38. Nieman, D.C., Henson, D.A., McAnulty, S.R. et al. (2002b). Influence of vitamin C supplementation on oxidative and immune changes following an ultramarathon. J. Appl. Physiol. 92, 1970–1977.PubMedGoogle Scholar
  39. Nieman, D.C., Henson, D.A., McAnulty, S.R. et al. (2004). Vitamin E and immunity after the Kona Triathlon World Championship. Med. Sci. Sports Exerc. 36, 1328–1335.CrossRefPubMedGoogle Scholar
  40. Nieman, D.C., Henson, D.A., Smith, L.L. et al. (2001). Cytokine changes after a marathon race. J. Appl. Physiol. 91, 109–114.PubMedGoogle Scholar
  41. Nieman, D.C., Johansen, L.M., Lee, J.W., Cermak, J., and Arabatzis, K. (1990). Infectious episodes in runners before and after the Los Angeles Marathon. J. Sports Med. Phys. Fit. 30, 316–328.Google Scholar
  42. Nieman, D.C., Oley, K., Henson, D.A. et al. (2006c). Ibuprofen use, endotoxemia, inflammation, and plasma cytokines during ultramarathon competition. Brain Beh. Immun. 20, 578–584.CrossRefGoogle Scholar
  43. Ostrowski, K., Schjerling, P., and Pedersen, B.K. (2000). Physical activity and plasma interleukin-6 in humans-effect of intensity of exercise. Eur. J. Appl. Physiol. 83, 512–515.CrossRefPubMedGoogle Scholar
  44. Palmer, F.M., Nieman, D.C., Henson, D.A. et al. (2003). Influence of vitamin C supplementation on oxidative and salivary IgA changes following an ultramarathon. Eur. J. Appl. Physiol. 89, 100–107.CrossRefPubMedGoogle Scholar
  45. Peters, E.M. and Bateman, E.D. (1983). Ultramarathon running and upper respiratory tract infections. An epidemiological survey. S. Afr. Med. J. 64, 582–584.PubMedGoogle Scholar
  46. Peterson, J.M., Trappe, T.A., Mylona, E. et al. (2003). Ibuprofen and acetaminophen, effect on muscle inflammation after eccentric exercise. Med. Sci. Sports Exerc. 35, 892–896.CrossRefPubMedGoogle Scholar
  47. Pizza, F.X., Cavender, D., Stockard, A., Baylies, H., and Beighle, A. (1999). Anti-inflammatory doses of ibuprofen, effect on neutrophils and exercise-induced muscle injury. Int. J. Sports Med. 20, 98–102.PubMedGoogle Scholar
  48. Peake, J.M. (2002). Exercise-induced alterations in neutrophil degranulation and respiratory burst activity: possible mechanisms of action. Exerc. Immunol. Rev. 8, 49–100.PubMedGoogle Scholar
  49. Powers, S.K., DeRuisseau, K.C., Quindry, J., and Hamilton, K.L. (2004). Dietary antioxidants and exercise. J. Sports Sci. 22, 81–94.CrossRefPubMedGoogle Scholar
  50. Quindry, J.C., McAnulty, S.R., Hudson, M.B. et al. (2008). Oral quercetin supplementation and blood oxidative stress during ultra-marathon competition. Int. J. Sports Nutr. Exerc. Metab. 18, 601–616.Google Scholar
  51. Ryan, A.J., Chang, R.T., and Gisolfi, C.V. (1996). Gastrointestinal permeability following aspirin intake and prolonged running. Med. Sci. Sports Exerc. 28, 698–705.PubMedGoogle Scholar
  52. Smetanka, R.D., Lambert, G.P., Murray, R., Eddy, D., Horn, M., and Gisolfi, C.V. (1999). Intestinal permeability in runners in the 1996 Chicago marathon. Int. J. Sports Nutr. 9, 426–433.Google Scholar
  53. Steensberg, A. (2003). The role of IL-6 in exercise-induced immune changes and metabolism. Exerc. Immunol. Rev. 9, 40–47.PubMedGoogle Scholar
  54. Steensberg, A., Keller, C., Hillig, T. et al. (2007). Nitric oxide production is a proximal signaling event controlling exercise-induced mRNA expression in human skeletal muscle. FASEB J. 21, 2683–2694.CrossRefPubMedGoogle Scholar
  55. Steerenberg, P.A., Van Asperen, I.A., Van Nieuw Amerongen, A., Biewenga, A., Mol, D., and Medema, G.J. (1997). Salivary levels of immunoglobulin A in triathletes. Eur. J. Oral Sci. 105, 305–309.CrossRefPubMedGoogle Scholar
  56. Steinacker, J.M., Lormes, W., Reissnecker, S., and Liu, Y. (2004). New aspects of the hormone and cytokine response to training. Eur. J. Appl. Physiol. 91, 382–391.CrossRefPubMedGoogle Scholar
  57. Suzuki, K., Nakaji, S., Yamada, M., Totsuka, M., Sato, K., and Sugawara, K. (2002). Systemic inflammatory response to exhaustive exercise. Cytokine kinetics. Exerc. Immunol. Rev. 8, 6–48.PubMedGoogle Scholar
  58. Suzuki, K., Nakaji, S., Yamada, M. et al. (2003). Impact of a competitive marathon race on systemic cytokine and neutrophil responses. Med. Sci. Sports Exerc. 35, 348–355.CrossRefPubMedGoogle Scholar
  59. Suzuki, K., Totsuka, M., Nakaji, S. et al. (1999). Endurance exercise causes interaction among stress hormones, cytokines, neutrophil dynamics, and muscle damage. J. Appl. Physiol. 87, 1360–1367.PubMedGoogle Scholar
  60. Tomasi, T.B., Trudeau, F.B., Czerwinski, D., and Erredge, S. (1982). Immune parameters in athletes before and after strenuous exercise. J. Clin. Immunol. 2, 173–178.CrossRefPubMedGoogle Scholar
  61. Trappe, T.A., White, F., Lambert, C.P., Cesar, D., Hellerstein, M., and Evans, W.J. (2002). Effect of ibuprofen and acetaminophen on postexercise muscle protein synthesis. Am. J. Endrocrin. Metab. 282, E551–E556.Google Scholar
  62. Van Nieuwenhoven, M.A., Brouns, F., and Brummer, R.J.M. (2004). Gastrointestinal profile of symptomatic athletes at rest and during physical exercise. Eur. J. Appl. Physiol. 91, 429–434.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  1. 1.Appalachian State UniversityBooneUSA
  2. 2.Department of Health and Exercise ScienceAppalachian State UniversityBooneUSA

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