Exercise and the Immune System

Chapter

Abstract

This chapter is divided into three major parts. The first part covers how exercise is associated with respiratory infection. Exercise’s effect on mucosal immunity, allergic rhinitis and airway inflammation is discussed as well as how certain viruses can affect respiratory infection risk in the athletic population. In the chapter’s second section, the influence of acute exercise on our immune system is explored. More specifically, the alterations in the innate immune system and acquired immune system in response to exercise and the mechanisms leading to these alterations are elucidated. Finally, the third part is on the effects of chronic exercise on the immune system. In this part, the beneficial anti-inflammatory effect of regular physical activity and health implication that this has on prevention and treatment of various diseases, which includes cancer, dementia, cardiovascular and pulmonary diseases, is discussed. In addition, the potential harmful effects of a high-intensity training period are also addressed. There is little research in these areas with resistance-type exercise, and unless stated otherwise, the studies mentioned here are with endurance-type exercise, such as running, rowing, cycling and swimming.

References

  1. Akimoto T, Kumai Y, Akama T et al (2003) Effects of 12 months of exercise training on salivary secretory IgA levels in elderly subjects. Br J Sports Med 37:76–79PubMedCentralPubMedCrossRefGoogle Scholar
  2. Akira S, Hemmi H (2003) Recognition of pathogen-associated molecular patterns by TLR family. Immunol Lett 85(2):85–95PubMedCrossRefGoogle Scholar
  3. Allgrove JE, Gomes E, Hough J, Gleeson M (2008) Effects of exercise intensity on salivary antimicrobial proteins and markers of stress in active men. J Sports Sci 26:653–661PubMedCrossRefGoogle Scholar
  4. Bate SL, Dollard SC, Cannon MJ (2010) Cytomegalovirus seroprevalence in the United States: the national health and nutrition examination surveys, 1988–2004. Clin Infect Dis 50(11):1439–1447PubMedCrossRefGoogle Scholar
  5. Bates DV (2005) Ambient ozone and mortality. Epidemiology 16(4):427–429PubMedCrossRefGoogle Scholar
  6. Beavers KM, Brinkley TE, Nicklas BJ (2010) Effect of exercise training on chronic inflammation. Clin Chim Acta 411(11–12):785–793PubMedCentralPubMedCrossRefGoogle Scholar
  7. Belda J, Ricart S, Casan P et al (2008) Airway inflammation in the elite athlete and type of sport. Br J Sports Med 42(4):244–248PubMedCrossRefGoogle Scholar
  8. Benshop RJ, Rodriguez-Feuerhahn M, Schedlowski M (1996) Catecholamine-induced leukocytosis: early observations, current research, and future directions. Brain Behav Immun 10:77–91CrossRefGoogle Scholar
  9. Bishop NC (2006) Acute exercise and acquired immune function. In: Gleeson M (ed) Immune function in sport and exercise, 1st edn. Churchill Livingstone/Elsevier, Edinburgh, pp 91–113CrossRefGoogle Scholar
  10. Bishop NC, Gleeson M (2009) Acute and chronic effects of exercise on markers of mucosal immunity. Front Biosci 14:4444–4456CrossRefGoogle Scholar
  11. Bishop NC, Blannin AK, Armstrong E et al (2000) Carbohydrate and fluid intake affect the saliva flow rate and IgA response to cycling. Med Sci Sports Exerc 32:2046–2051PubMedCrossRefGoogle Scholar
  12. Bishop NC, Walsh N, Scanlon GA (2003) Effect of prolonged exercise and carbohydrate on total neutrophil elastase content. Med Sci Sports Exerc 35(8):1326–1332PubMedCrossRefGoogle Scholar
  13. Blannin AK (2006) Acute exercise and innate immune function. In: Gleeson M (ed) Immune function in sport and exercise, 1st edn. Churchill Livingstone/Elsevier, Edinburgh, pp 67–89CrossRefGoogle Scholar
  14. Blannin AK, Robson PJ, Walsh NP et al (1998) The effect of exercising to exhaustion at different intensities on saliva immunoglobulin A, protein and electrolyte secretion. Int J Sports Med 19:547–552PubMedCrossRefGoogle Scholar
  15. Blomberg A (2000) Airway inflammatory and antioxidant responses to oxidative and particulate air pollutants – experimental exposure studies in humans. Clin Exp Allergy 30:310–317PubMedCrossRefGoogle Scholar
  16. Bonsignore MR, Morici G, Riccobono L et al (2001) Airway inflammation in nonasthmatic amateur runners. Am J Physiol Lung Cell Mol Physiol 281:668–676Google Scholar
  17. Booth S, Florida‐James G, McFarlin B (2010) The impact of acute strenuous exercise on TLR2, TLR4 and HLA.DR expression on human blood monocytes induced by autologous serum. Eur J Appl Physiol 110(6):1259–1268PubMedCrossRefGoogle Scholar
  18. Bosch JA, Ring C, de Geus EJC, Veerman ECI, Nieuw Amerogen AV (2002) Stress and secretory immunity. Int Rev Neurobiol 52:213–253Google Scholar
  19. Bougault V, Turmel J, St-Laurent J et al (2009) Asthma, airway inflammation and epithelial damage in swimmers and cold-air athletes. Eur Respir J 33(4):740–746PubMedCrossRefGoogle Scholar
  20. Bougault V, Turmel J, Boulet LP (2010) Bronchial challenges and respiratory symptoms in elite swimmers and winter sport athletes: airway hyperresponsiveness in asthma: its measurement and clinical significance. Chest 138:31S–37SPubMedCrossRefGoogle Scholar
  21. Boulet LP, Turcotte H, Langdeau JB, Bernier MC (2005a) Lower airway inflammatory responses to high-intensity training in athletes. Clin Invest Med 28(1):15–22PubMedGoogle Scholar
  22. Boulet LP, Prince P, Turcotte H (2005b) Clinical features and airway inflammation in mild asthma versus asymptomatic airway hyperresponsiveness. Respir Med 100(2):292–299PubMedCrossRefGoogle Scholar
  23. Britt W (2008) Manifestations of human cytomegalovirus infection: proposed mechanisms of acute and chronic disease. Curr Top Microbiol Immunol 325:417–470PubMedGoogle Scholar
  24. Brown J, Wang H, Hajishengallis GN et al (2011) TLR-signaling Networks. J Dent Res 90(4):417–427PubMedCentralPubMedCrossRefGoogle Scholar
  25. Brunekreef B, Holgatek ST (2002) Air pollution and health. Lancet 360:1233–1242PubMedCrossRefGoogle Scholar
  26. Camous L, Roumenina L, Bigot S et al (2011) Complement alternative pathway acts as a positive feedback amplification of neutrophil activation. Blood 117(4):1340–1349PubMedCrossRefGoogle Scholar
  27. Carins J, Booth C (2002) Salivary immunoglobulin-A as a marker of stress during strenuous physical training. Aviat Space Environ Med 73:1203–1207PubMedGoogle Scholar
  28. Chang CM, Yu KJ, Mbulaiteye SM et al (2009) The extent of genetic diversity of Epstein-Barr virus and its geographic and disease patterns: a need for reappraisal. Virus Res 143:209–221PubMedCentralPubMedCrossRefGoogle Scholar
  29. Chatterton RT, Vogelsong KM, Lu YC et al (1996) Salivary alpha-amylase as a measure of endogenous adrenergic activity. Clin Physiol 16:433–448PubMedCrossRefGoogle Scholar
  30. Chicharro JL, Lucía A, Peréz M et al (1998) Saliva composition and exercise. Sports Med 26:17–27PubMedCrossRefGoogle Scholar
  31. Chinda D, Nakaji S, Umeda T et al (2003) A competitive marathon race decreases neutrophil functions in athletes. Luminescence 18(6):324–329PubMedCrossRefGoogle Scholar
  32. Chow CW, Abreu MTH, Suzuki T, Downey GP (2003) Oxidative stress and acute lung injury. Am J Respir Cell Mol Biol 29(4):427–431PubMedCrossRefGoogle Scholar
  33. Chung HY, Lee EK, Choi YJ et al (2011) Molecular inflammation as an underlying mechanism of the aging process and age-related diseases. J Dent Res 90(7):830–840PubMedCrossRefGoogle Scholar
  34. Cockcroft DW, Davis BE (2006) Mechanisms of airway hyperresponsiveness. J Allergy Clin Immunol 118:551–559PubMedCrossRefGoogle Scholar
  35. Coen PM, Flynn MG, Markofski MM et al (2010) Adding exercise to rosuvastatin treatment: influence on C-reactive protein, monocyte toll-like receptor 4 expression, and inflammatory monocyte (CD14+CD16+) population. Metabolism 59:1775–1783PubMedCrossRefGoogle Scholar
  36. Cox AJ, Gleeson M, Pyne DB et al (2004) Valtrex therapy for Epstein-Barr virus reactivation and upper respiratory symptoms in elite runners. Med Sci Sports Exerc 36:1104–1110PubMedCrossRefGoogle Scholar
  37. Cox AJ, Gleeson M, Pyne DB et al (2008) Clinical and laboratory evaluation of upper respiratory symptoms in elite athletes. Clin J Sport Med 18:438–445PubMedCrossRefGoogle Scholar
  38. D'Alonzo GE Jr (2002) Scope and impact of allergic rhinitis. J Am Osteopath Assoc 102(6 Suppl 2):S2–S6PubMedGoogle Scholar
  39. Denguezli M, Chiekh IB, Saad HB (2008) One-year endurance training: effects on lung function and airway inflammation. J Sports Sci 26(12):1351–1359PubMedCrossRefGoogle Scholar
  40. Discacciati A, Wolk A (2014) Lifestyle and dietary factors in prostate cancer prevention. Recent Results Cancer Res 202:27–37PubMedCrossRefGoogle Scholar
  41. Dykewicz MS, Hamilos DL (2010) Rhinitis and sinusitis. J Allergy Clin Immunol 125(2 Suppl 2):S103–S115PubMedCrossRefGoogle Scholar
  42. Engebretsen L, Steffen K, Alonso JM et al (2010) Sports injuries and illnesses during the Winter Olympic Games 2010. Br J Sports Med 44(11):772–780PubMedCrossRefGoogle Scholar
  43. Fahlman MM, Engels HJ (2005) Mucosal IgA and URTI in American college football players: a year longitudinal study. Med Sci Sports Exerc 37:374–380PubMedCrossRefGoogle Scholar
  44. Febbraio MA, Pedersen BK (2002) Muscle-derived interleukin-6: mechanisms for activation and possible biological roles. FASEB J 16(11):1335–1347PubMedCrossRefGoogle Scholar
  45. Fisher-Wellman K, Bloomer RJ (2009) Acute exercise and oxidative stress: a 30 year history. Dyn Med 8(1):1–25PubMedCentralPubMedCrossRefGoogle Scholar
  46. Flynn MG, McFarlin BK, Phillips MD et al (2003) Toll-like receptor 4 and CD14 mRNA expression are lower in resistive exercise-trained elderly women. J Appl Physiol 95:1833–1842PubMedCrossRefGoogle Scholar
  47. Foster NK, Martyn JB, Rangno RE et al (1986) Leukocytosis of exercise: role of cardiac output and catecholamines. J Appl Physiol 61(6):2218–2223PubMedGoogle Scholar
  48. Fry RW, Morton AR, Crawford GP, Keast D (1992) Cell numbers and in vitro responses of leucocytes and lymphocyte subpopulations following maximal exercise and interval training sessions of different intensities. Eur J Appl Physiol Occup Physiol 64:218–227PubMedCrossRefGoogle Scholar
  49. Gabriel H, Urhausen A, Kindermann W (1991) Circulating leucocyte and lymphocyte subpopulations before and after intensive endurance exercise to exhaustion. Eur J Appl Physiol Occup Physiol 63(6):449–457PubMedCrossRefGoogle Scholar
  50. Gabriel H, Urhausen A, Kindermann W (1992) Mobilization of circulating leucocyte and lymphocyte subpopulations during and after short, anaerobic exercise. Eur J Appl Physiol Occup Physiol 65(2):164–170PubMedCrossRefGoogle Scholar
  51. Giraldo E, Garcia JJ, Hinchado MD, Ortega E (2009) Exercise intensity-dependent changes in the inflammatory response in sedentary women: role of neuroendocrine parameters in the neutrophil phagocytic process and the pro-/anti-inflammatory cytokine balance. Neuroimmunomodulation 16(4):237–244PubMedCrossRefGoogle Scholar
  52. Gkrania-Klotsas E, Langenberg C, Sharp SJ et al (2013) Seropositivity and higher immunoglobulin g antibody levels against cytomegalovirus are associated with mortality in the population-based European prospective investigation of Cancer-Norfolk cohort. Clin Infect Dis 56(10):1421–1427PubMedCentralPubMedCrossRefGoogle Scholar
  53. Gleeson M (2006) Introduction to the immune system. In: Gleeson M (ed) Immune function in sport and exercise, 1st edn. Churchill Livingstone/Elsevier, Edinburgh, pp 15–44CrossRefGoogle Scholar
  54. Gleeson M, Bishop NC (2005) The T cell and NK cell immune response to exercise. Ann Transplant 10(4):43–48PubMedGoogle Scholar
  55. Gleeson M, Pyne DB (2000) Special feature for the Olympics: effects of exercise on the immune system: exercise effects on mucosal immunity. Immunol Cell Biol 78:536–544PubMedCrossRefGoogle Scholar
  56. Gleeson M, Robson-Ansley P (2006) Immune responses to intensified training and overtraining. In: Gleeson M (ed) Immune function in sport and exercise, 1st edn. Churchill Livingstone/Elsevier, Edinburgh, pp 91–113Google Scholar
  57. Gleeson M, McDonald WA, Cripps AW et al (1995) The effect on immunity of long-term intensive training in elite swimmers. Clin Exp Immunol 102:210–216PubMedCentralPubMedCrossRefGoogle Scholar
  58. Gleeson M, McDonald WA, Pyne DB et al (1999) Salivary IgA levels and infection risk in elite swimmers. Med Sci Sports Exerc 31:67–73PubMedCrossRefGoogle Scholar
  59. Gleeson M, Pyne DB, Austin JP et al (2002) Epstein-Barr virus reactivation and upper-respiratory illness in elite swimmers. Med Sci Sports Exerc 34:411–417PubMedCrossRefGoogle Scholar
  60. Gleeson M, Pyne DB, Callister R (2004) The missing links in exercise effects on mucosal immunity. Exerc Immunol Rev 4:107–128Google Scholar
  61. Gleeson M, McFarlin B, Flynn M (2006) Exercise and Toll-like receptors. Exerc Immunol Rev 12:34–53PubMedGoogle Scholar
  62. Gleeson M, Bishop NC, Stensel DJ et al (2011) The anti-inflammatory effects of exercise: mechanisms and implications for the prevention and treatment of disease. Nat Rev Immunol 11:607–615PubMedCrossRefGoogle Scholar
  63. Gomes EC, Stone V, Florida-James G (2010) Investigating performance and lung function in a hot, humid and ozone-polluted environment. Eur J Appl Physiol 110(1):199–205PubMedCrossRefGoogle Scholar
  64. Gomes EC, Stone V, Florida-James G (2011) Impact of heat and pollution on oxidative stress and CC16 secretion after 8 km run. Eur J Appl Physiol 111(9):2089–2097PubMedCrossRefGoogle Scholar
  65. Gomes EC, Silva AN, de Oliveira MR (2012) Oxidants, antioxidants, and the beneficial roles of exercise-induced production of reactive species. Oxid Med Cell Longev 2012:756132PubMedCentralPubMedGoogle Scholar
  66. Gomez-Cabrera MC, Domenech E, Viña J (2008) Moderate exercise is an antioxidant: upregulation of antioxidant genes by training. Free Radic Biol Med 44(2):126–131PubMedCrossRefGoogle Scholar
  67. Gratas-Delamarche A, Derbré F, Vincent S, Cillard J (2014) Physical inactivity, insulin resistance, and the oxidative-inflammatory loop. Free Radic Res 48(1):93–108PubMedCrossRefGoogle Scholar
  68. Hack V, Strobel G, Weiss M, Weicker H (1994) PMN cell counts on phagocytic activity of highly trained athletes depend on training period. J Appl Physiol 77(4):1731–1735PubMedGoogle Scholar
  69. Halliwell B, Gutteridge JMC (2007) Free radicals in biology and medicine. Oxford University Press, New YorkGoogle Scholar
  70. Helenius I, Lumme A, Haahtela T (2005) Asthma, airway inflammation and treatment in elite athletes. Sports Med 35(7):565–574PubMedCrossRefGoogle Scholar
  71. Heymann EP, Goldsmith D (2012) Best approaches in the battle against Globesity? Learning lessons from our experience tackling HIV-AIDS and tobacco smoking. JRSM Short Rep 3(7):45PubMedCentralPubMedCrossRefGoogle Scholar
  72. Hochberg D, Souza T, Catalina M et al (2004) Acute infection with Epstein-Barr virus targets and overwhelms the peripheral memory B-cell compartment with resting, latently infected cells. J Virol 78(10):5194–5204PubMedCentralPubMedCrossRefGoogle Scholar
  73. Hoffman-Goetz L, Simpson JR, Cipp N et al (1990) Lymphocyte subset responses to repeated submaximal exercise in men. J Appl Physiol 68(3):1069–1074PubMedGoogle Scholar
  74. IARC (2002) Handbooks of cancer prevention. In: Weight control and physical activity, vol 6. IARC press, LyonGoogle Scholar
  75. Jarvis MA, Nelson JA (2002) Mechanisms of human cytomegalovirus persistence and latency. Front Biosci 7:d1575–d1582PubMedCrossRefGoogle Scholar
  76. Kakanis MW, Peake J, Brenu EW et al (2010) The open window of susceptibility to infection after acute exercise in healthy young male elite athletes. Exerc Immunol Rev 16:119–137PubMedGoogle Scholar
  77. Kappel M, Tvede N, Galbo H et al (1991) Evidence that the effect of physical exercise on NK cell activity is mediated by epinephrine. J Appl Physiol 70:2530–2534PubMedGoogle Scholar
  78. Kivlighan KT, Granger DA (2006) Salivary alpha-amylase response to competition: Relation to gender, previous experience, and attitudes. Psychoneuroendocrinology 31:703–714PubMedCrossRefGoogle Scholar
  79. Klentrou P, Cieslak T, MacNeil M et al (2002) Effect of moderate exercise on salivary immunoglobulin A and infection risk in humans. Eur J Appl Physiol 87:153–158PubMedCrossRefGoogle Scholar
  80. Koch A (2010) Immune response to resistance exercise. Am J Lifestyle Med 4:244–252CrossRefGoogle Scholar
  81. Kostka T, Berthouze SE, Lacour J, Bonnefoy M (2000) The symptomatology of upper respiratory tract infections and exercise in elderly people. Med Sci Sports Exerc 32(1):46–51PubMedCrossRefGoogle Scholar
  82. Lamm ME (1998) Current concepts in mucosal immunity IV. How epithelial transport of IgA antibodies relates to host defense. Am J Physiol 274:G614–G617PubMedGoogle Scholar
  83. Lancaster GI, Halson SL, Khan Q et al (2004) Effects of acute exhaustive exercise and chronic exercise training on type 1 and type 2 T lymphocytes. Exerc Immunol Rev 10:91–106PubMedGoogle Scholar
  84. Lancaster GI, Khan Q, Drysdale P et al (2005a) The physiological regulation of toll-like receptor expression and function in humans. J Physiol 563(3):945–955PubMedCentralPubMedCrossRefGoogle Scholar
  85. Lancaster GI, Khan Q, Drysdale PT et al (2005b) Effect of prolonged exercise and carbohydrate ingestion on type 1 and type 2 T lymphocyte distribution and intracellular cytokine production in humans. J Appl Physiol 98(2):565–571PubMedCrossRefGoogle Scholar
  86. Langdeau JB, Turcotte H, Bowie DM et al (2000) Airway hyperresponsiveness in elite athletes. Am J Respir Crit Care Med 161(5):1479–1484PubMedCrossRefGoogle Scholar
  87. Lee I, Oguma Y (2006) Physical activity. In: Schottenfeld D, Fraumeni JF (eds) Cancer epidemiology and prevention, 3rd edn. Oxford University Press, New YorkGoogle Scholar
  88. Lee S, Kuk JL, Davidson LE et al (2005) Exercise without weight loss is an effective strategy for obesity reduction in obese individuals with and without Type 2 diabetes. J Appl Physiol 99:1220–1225PubMedCrossRefGoogle Scholar
  89. Leggate M, Nowell MA, Jones SA, Nimmo MA (2010) The response of interleukin-6 and soluble interleukin-6 receptor isoforms following intermittent high intensity and continuous moderate intensity cycling. Cell Stress Chaperones 15(6):827–833PubMedCentralPubMedCrossRefGoogle Scholar
  90. Lewicki R, Tchórzewski H, Denys A et al (1987) Effect of physical exercise on some parameters of immunity in conditioned sportsmen. Int J Sports Med 8(5):309–314PubMedCrossRefGoogle Scholar
  91. Li TL, Gleeson M (2004) The effect of single and repeated bouts of prolonged cycling and circadian variation on saliva flow rate, immunoglobulin A and alpha-amylase responses. J Sports Sci 22:1015–1024PubMedCrossRefGoogle Scholar
  92. Libicz S, Mercier B, Bigou N, Le Gallais D, Castex F (2006) Salivary IgA response of triathletes participating in the French Iron Tour. Int J Sports Med 27(5):389–394Google Scholar
  93. Matthews CE, Ockene IS, Freedson PS et al (2002) Moderate to vigorous physical activity and risk of upper-respiratory tract infection. Med Sci Sports Exerc 34(8):1242–1248PubMedCrossRefGoogle Scholar
  94. McCarthy DA, Dale MM (1998) The leucocytosis of exercise. A review and model. Sports Med 6(6):333–363CrossRefGoogle Scholar
  95. McCarthy DA, Macdonald I, Grant M et al (1992) Studies on the immediate and delayed leucocytosis elicited by brief (30-min) strenuous exercise. Eur J Appl Physiol Occup Physiol 64:513–517PubMedCrossRefGoogle Scholar
  96. McFarlin BK, Flynn MG, Stewart LK, Timmerman KL (2004a) Carbohydrate intake during endurance exercise increases natural killer cell responsiveness to IL-2. J Appl Physiol 96(1):271–275PubMedCrossRefGoogle Scholar
  97. McFarlin BK, Flynn MG, Campbell WW et al (2004b) TLR4 is lower in resistance-trained older women and related to inflammatory cytokines. Med Sci Sports Exerc 36(11):1876–1883PubMedCrossRefGoogle Scholar
  98. Miles MP, Kraemer WJ, Nindl BC et al (2003) Strength, workload, anaerobic intensity and the immune response to resistance exercise in women. Acta Physiol Scand 178(2):155–163PubMedCrossRefGoogle Scholar
  99. Mooren FC, Blöming D, Lechtermann A et al (2002) Lymphocyte apoptosis after exhaustive and moderate exercise. J Appl Physiol 93(1):147–153PubMedCrossRefGoogle Scholar
  100. Morice G, Bonsignore MR, Zangala D et al (2004) Airway cell composition at rest and after an all-out test in competitive runners. Med Sci Sports Exerc 36(10):1723–1729CrossRefGoogle Scholar
  101. Murphy EA, Davis JM, Brown AS et al (2004) Effects of moderate exercise and oat beta-glucan on lung tumor metastases and macrophage antitumor cytotoxicity. J Appl Physiol 97(3):955–959PubMedCrossRefGoogle Scholar
  102. Naci H, Ioannidis JP (2013) Comparative effectiveness of exercise and drug interventions on mortality outcomes: metaepidemiological study. BMJ 347:f5577PubMedCentralPubMedCrossRefGoogle Scholar
  103. Nair S (2012) Nasal breathing exercise and its effect on symptoms of allergic rhinitis. Indian J Otolaryngol Head Neck Surg 64(2):172–176PubMedCentralPubMedCrossRefGoogle Scholar
  104. Nater UM, La Marca R, Florin L et al (2006) Stress-induced changes in human salivary alpha-amylase activity - associations with adrenergic activity. Psychoneuroendocrinology 31:49–58PubMedCrossRefGoogle Scholar
  105. Neville V, Gleeson M, Folland JP (2008) Salivary IgA as a risk factor for upper respiratory infections in elite professional athletes. Med Sci Sports Exerc 40:1228–1236PubMedCrossRefGoogle Scholar
  106. Nguyen HQ, Chu L, Liu IL et al (2014) Associations between physical activity and 30-Day readmission risk in chronic obstructive pulmonary disease. Ann Am Thorac Soc 11(5):695–705PubMedCrossRefGoogle Scholar
  107. Nieman DC (1994) Exercise, infection and immunity. Int J Sports Med 15:S131–S141PubMedCrossRefGoogle Scholar
  108. Nieman DC (2000) Is infection risk linked to exercise workload? Med Sci Sports Exerc 32:S406–S411PubMedCrossRefGoogle Scholar
  109. Nieman DC, Bishop NC (2006) Nutritional strategies to counter stress to the immune system in athletes, with special reference to football. J Sports Sci 24(7):763–772PubMedCrossRefGoogle Scholar
  110. Nieman DC, Nehlsen-Cannarella SL, Markoff PA et al (1990) The effects of moderate exercise training on natural killer cells and acute upper respiratory tract infections. Int J Sports Med 11(6):467–473PubMedCrossRefGoogle Scholar
  111. Nieman DC, Miller AR, Henson DA et al (1993) Effects of high- vs moderate-intensity exercise on natural killer cell activity. Med Sci Sports Exerc 25(10):1126–1134PubMedCrossRefGoogle Scholar
  112. Nieman DC, Nehlsen-Cannarella SL, Fagoaga OR et al (1998) Effects of mode and carbohydrate on the granulocyte and monocyte response to intensive, prolonged exercise. J Appl Physiol 84(4):1252–1259PubMedGoogle Scholar
  113. Nieman DC, Henson DA, Fagoaga OR et al (2002) Change in salivary IgA following a competitive marathon race. Int J Sports Med 23:69–75PubMedCrossRefGoogle Scholar
  114. Niess AM, Simon P (2007) Response and adaptation of skeletal muscle to exercise—the role of reactive oxygen species. Front Biosci 12:4826–4838PubMedCrossRefGoogle Scholar
  115. Nimmo MA, Leggate M, Viana JL, King JA (2013) The effect of physical activity on mediators of inflammation. Diabetes Obes Metab 15(Suppl 3):51–60PubMedCrossRefGoogle Scholar
  116. Okutsu M, Suzuki K, Ishijima T et al (2008) The effects of acute exercise-induced cortisol on CCR2 expression on human monocytes. Brain Behav Immun 22(7):1066–1071PubMedCrossRefGoogle Scholar
  117. Oliveira-Child M, Leggate M, Gleeson M (2013) Effects of two weeks of high-intensity interval training (HIIT) on monocyte TLR2 and TLR4 expression in high BMI sedentary Men. Int J Exerc Sci 6:81–90Google Scholar
  118. Ortega E, Collazos ME, Maynar M et al (1993) Stimulation of the phagocytic function of neutrophils in sedentary men after acute moderate exercise. Eur J Appl Physiol Occup Physiol 66(1):60–64PubMedCrossRefGoogle Scholar
  119. Ortega E, Forner MA, Barriga C (1997) Exercise-induced stimulation of murine macrophage chemotaxis: role of corticosterone and prolactin as mediators. J Physiol 498(Pt 3):729–734PubMedCentralPubMedCrossRefGoogle Scholar
  120. Ortega E, Marchena JM, García JJ et al (2005) Norepinephrine as mediator in the stimulation of phagocytosis induced by moderate exercise. Eur J Appl Physiol 93(5–6):714–718PubMedCrossRefGoogle Scholar
  121. Ostrowski K, Rohde T, Zacho M et al (1998) Evidence that IL-6 is produced in skeletal muscle during intense long-term muscle activity. J Physiol 508:949–953PubMedCentralPubMedCrossRefGoogle Scholar
  122. Ostrowski K, Rohde T, Asp S et al (2001) Chemokines are elevated in plasma after strenuous exercise. Eur J Cell Physiol 84:244–245CrossRefGoogle Scholar
  123. Palmer FM, Nieman DC, Henson DA et al (2003) Influence of vitamin C supplementation on oxidative and salivary IgA changes following an ultramarathon. Eur J Appl Physiol 89:100–107PubMedCrossRefGoogle Scholar
  124. Peake JM (2002) Exercise-induced alterations in neutrophil degranulation and respiratory burst activity: possible mechanisms of action. Exerc Immunol Rev 8:49–100PubMedGoogle Scholar
  125. Peake J, Suzuki K (2004) Neutrophil activation, antioxidant supplements and exercise induced oxidative stress. Exerc Immunol Rev 10:129–141PubMedGoogle Scholar
  126. Pedersen L (2009) Airway hyperresponsiveness and airway inflammation in elite swimmers. Clin Respir J 3(1):62CrossRefGoogle Scholar
  127. Pedersen BK, Fischer CP (2007) Beneficial health effects of exercise–the role of IL-6 as a myokine. Trends Pharmacol Sci 28(4):152–156PubMedCrossRefGoogle Scholar
  128. Pedersen BK, Bruunsgaard H, Klokker M et al (1997) Exercise-induced immunomodulation – possible roles of neuroendocrine and metabolic factors. Int J Sports Med 18(Suppl 1):S2–S7PubMedCrossRefGoogle Scholar
  129. Pedersen BK, Steensberg A, Schjerling P (2001) Muscle-derived interleukin-6: possible biological effects. J Physiol 536(Pt 2):329–337PubMedCentralPubMedCrossRefGoogle Scholar
  130. Peel JB, Sui X, Adams SA et al (2009a) A prospective study of cardiorespiratory fitness and breast cancer mortality. Med Sci Sports Exerc 41(4):742–748PubMedCentralPubMedCrossRefGoogle Scholar
  131. Peel JB, Sui X, Matthews CE et al (2009b) Cardiorespiratory fitness and digestive cancer mortality: findings from the aerobics center longitudinal study. Cancer Epidemiol Biomarkers Prev 18(4):1111–1117PubMedCentralPubMedCrossRefGoogle Scholar
  132. Proctor GB, Garrett JR, Carpenter GH, Ebersole LE (2003) Salivary secretion of immunoglobulin A by submandibular glands in response to autonomimetic infusions in anaesthetised rats. J Neuroimmunol 136:17–24PubMedCrossRefGoogle Scholar
  133. Pue CA, Mortensen RF, Marsh CB et al (1996) Acute phase levels of C-reactive protein enhance IL-1 beta and IL-1ra production by human blood monocytes but inhibit IL-1 beta and IL-1ra production by alveolar macrophages. J Immunol 156:1594–1600PubMedGoogle Scholar
  134. Pyne DB (1994) Regulation of neutrophil function during exercise. Sports Med 17(4):245–258PubMedCrossRefGoogle Scholar
  135. Pyne DB, Baker MS, Fricker PA et al (1995) Effects of an intensive 12-wk training program by elite swimmers on neutrophil oxidative activity. Med Sci Sports Exerc 27:536–542PubMedCrossRefGoogle Scholar
  136. Pyne D, McDonald W, Gleeson M et al (1999) Mucosal immunity, respiratory illness, and competitive performance in elite swimmers. Med Sci Sports Exerc 33:348–353CrossRefGoogle Scholar
  137. Pyne DB, Gleeson M, McDonald WA et al (2000) Training strategies to maintain immunocompetence in athletes. Int J Sports Med 21(suppl 1):S51–S60PubMedCrossRefGoogle Scholar
  138. Radák Z, Apor P, Pucsok J et al (2003) Marathon running alters the DNA base excision repair in human skeletal muscle. Life Sci 72(14):1627–1633PubMedCrossRefGoogle Scholar
  139. Radak Z, Chung HY, Goto S (2008) Systemic adaptation to oxidative challenge induced by regular exercise. Free Radic Biol Med 44(2):153–159PubMedCrossRefGoogle Scholar
  140. Reid VL, Gleeson M, Williams N, Clancy RL (2004) Clinical investigation of athletes with persistent fatigue and/or recurrent infections. Br J Sports Med 38:42–45PubMedCentralPubMedCrossRefGoogle Scholar
  141. Roberts ET, Haan MN, Dowd JB, Aiello AE (2010) Cytomegalovirus antibody levels, inflammation, and mortality among elderly Latinos over 9 years of follow-up. Am J Epidemiol 172(4):363–371PubMedCentralPubMedCrossRefGoogle Scholar
  142. Robson PJ, Blannin AK, Walsh NP et al (1999) Effects of exercise intensity, duration and recovery on in vitro neutrophil function in male athletes. Int J Sports Med 20(2):128–135PubMedGoogle Scholar
  143. Rodriguez AB, Barriga C, De la Fuente M (1991) Phagocytic function of blood neutrophils in sedentary Young people after physical exercise. Int J Sports Med 12(3):276–280PubMedCrossRefGoogle Scholar
  144. Roitt IM, Delves PJ (2001) Roitt’s essential immunology, 10th edn. Blackwell Science, LondonGoogle Scholar
  145. Ruedl G, Schobersberger W, Pocecco E et al (2012) Sport injuries and illnesses during the first Winter Youth Olympic Games 2012 in Innsbruck, Austria. Br J Sports Med 46(15):1030–1037PubMedCrossRefGoogle Scholar
  146. Sand KL, Flatebo T, Andersen MB et al (2013) Effects of exercise on leukocytosis and blood hemostasis in 800 healthy young females and males. World J Exp Med 3(1):11–20PubMedCentralPubMedCrossRefGoogle Scholar
  147. Sarin S, Undem B, Sanico A et al (2006) The role of the nervous system in rhinitis. J Allergy Clin Immunol 118(5):999–1016PubMedCrossRefGoogle Scholar
  148. Sari-Sarraf V, Reilly T, Doran DA (2006) Salivary IgA response to intermittent and continuous exercise. Int J Sports Med 27:849–855PubMedCrossRefGoogle Scholar
  149. Scannapieco FA, Torres G, Levine MJ (1993) Salivary alpha-amylase: role in dental plaque and caries formation. Crit Rev Oral Biol Med 4:301–307PubMedGoogle Scholar
  150. Scharhag J, Meyer T, Gabriel HH et al (2005) Does prolonged cycling of moderate intensity affect immune cell function? Br J Sports Med 39(3):171–177PubMedCentralPubMedCrossRefGoogle Scholar
  151. Schenkels LC, Veerman EC, Nieuw Amerongen AV (1995) Biochemical composition of human saliva in relation to other mucosal fluids. Crit Rev Oral Biol Med 6:161–175PubMedCrossRefGoogle Scholar
  152. Sen CK, Roy S (2001) Antioxidant regulation of cell adhesion. Med Sci Sports Exerc 33(3):377–381PubMedCrossRefGoogle Scholar
  153. Shephard RJ (2003) Adhesion molecules, catecholamines and leucocyte redistribution during and following exercise. Sports Med 33(4):261–284PubMedCrossRefGoogle Scholar
  154. Shephard RJ, Shek PN (1999) Effects of exercise and training on natural killer cell counts and cytolytic activity: a meta-analysis. Sports Med 28:177–195PubMedCrossRefGoogle Scholar
  155. Simanek AM, Dowd JB, Pawelec G et al (2011) Seropositivity to cytomegalovirus, inflammation, all-cause and cardiovascular disease-related mortality in the United States. PLoS One 6(2), e16103PubMedCentralPubMedCrossRefGoogle Scholar
  156. Simpson RJ, Florida-James GD, Whyte PG et al (2006) The effects of intensive, moderate and downhill treadmill running on human blood lymphocytes expressing the adhesion/activation molecules CD54 (ICAM-1), CD18 (B2 integrin) and CD53. Eur J Appl Physiol 97:109–121PubMedCrossRefGoogle Scholar
  157. Simpson RJ, McFarlin BK, McSporran C et al (2009) Toll-like receptor expression on classic and pro-inflammatory blood monocytes after acute exercise in humans. Brain Behav Immun 23(2):232–239PubMedCrossRefGoogle Scholar
  158. Slattery ML (2004) Physical activity and colorectal cancer. Sports Med 34(4):239–252PubMedCrossRefGoogle Scholar
  159. Smith LL (2000) Cytokine hypothesis of overtraining: a physiological adaptation to excessive stress? Med Sci Sports Exerc 32:317–331PubMedCrossRefGoogle Scholar
  160. Spence L, Brown WJ, Pyne DB et al (2007) Incidence, etiology, and symptomatology of upper respiratory illness in elite athletes. Med Sci Sports Exerc 39(4):577–586PubMedCrossRefGoogle Scholar
  161. Starkie RL, Rolland J, Febbraio MA (2001a) Effect of adrenergic blockade on lymphocyte cytokine production at rest and during exercise. Am J Physiol Cell Physiol 281(4):C1233–C1240PubMedGoogle Scholar
  162. Starkie RL, Rolland J, Angus DJ et al (2001b) Circulating monocytes are not the source of elevations in plasma IL-6 and TNF-alpha levels. Am J Physiol Cell Physiol 280(4):C769–C774PubMedGoogle Scholar
  163. Steensberg A, Morrow J, Toft AD et al (2002) Prolonged exercise, lymphocyte apoptosis and F2-isoprostanes. Eur J Appl Physiol 87:38–42Google Scholar
  164. Steerenberg PA, van Asperen IA, van Nieuw AA et al (1997) Salivary levels of immunoglobulin A in triathletes. Eur J Oral Sci 105:305–309PubMedCrossRefGoogle Scholar
  165. Stewart LK, Flynn MG, Campbell WW et al (2005) Influence of exercise training and age on CD14+ cell-surface expression of toll-like receptor 2 and 4. Brain Behav Immun 19:389–397PubMedCrossRefGoogle Scholar
  166. Sui X, Lee DC, Matthews CE et al (2010) Influence of cardiorespiratory fitness on lung cancer mortality. Med Sci Sports Exerc 42(5):872–878PubMedCentralPubMedCrossRefGoogle Scholar
  167. Sureda A, Cordova A, Ferrer MD et al (2009) Effects of L-citrulline oral supplementation on polymorphonuclear neutrophils oxidative burst and nitric oxide production after exercise. Free Radic Res 43(9):828–835PubMedCrossRefGoogle Scholar
  168. Suzui M, Kawai T, Kimura H, Takeda K et al (2004) Natural killer cell lytic activity and CD56(dim) and CD56(bright) cell distributions during and after intensive training. J Appl Physiol 96:2167–2173PubMedCrossRefGoogle Scholar
  169. Syu GD, Chen HI, Jen CJ (2012) Differential effects of acute and chronic exercise on human neutrophil functions. Med Sci Sports Exerc 44(6):1021–1027PubMedCrossRefGoogle Scholar
  170. Thorley-Lawson DA, Gross A (2004) Persistence of the Epstein-Barr virus and the origins of associated lymphomas. N Engl J Med 350:1328–1337PubMedCrossRefGoogle Scholar
  171. Thorley-Lawson DA, Hawkins JB, Tracy SI et al (2013) The pathogenesis of Epstein-Barr vírus persistent infection. Curr Opin Virol 3(3):227–232PubMedCentralPubMedCrossRefGoogle Scholar
  172. Tilg H, Dinarello CA, Mier JW (1997) IL-6 and APPs: anti-inflammatory and immunosuppressive mediators. Immunol Today 18:428–432PubMedCrossRefGoogle Scholar
  173. Timmerman KL, Flynn MG, Coen PM et al (2008) Exercise training-induced lowering of inflammatory (CD14+CD16+) monocytes: a role in the anti-inflammatory influence of exercise? J Leukoc Biol 84:1271–1278PubMedCrossRefGoogle Scholar
  174. Timmons BW, Cieslak T (2008) Human natural killer cell subsets and acute exercise: a brief review. Exerc Immunol Rev 14:8–23PubMedGoogle Scholar
  175. Tongtako W, Klaewsongkram J, Jaronsukwimal N et al (2012) The effect of acute exhaustive and moderate intensity exercises on nasal cytokine secretion and clinical symptoms in allergic rhinitis patients. Asian Pac J Allergy Immunol 30(3):185–192PubMedGoogle Scholar
  176. Toussirot E, Roudier J (2008) Epstein–Barr virus in autoimmune diseases. Best Pract Res Clin Rheumatol 22(5):883–896PubMedCrossRefGoogle Scholar
  177. Tvede N, Kappel M, Klarlund K et al (1994) Evidence that the effect of bicycle exercise on blood mononuclear cell proliferative responses and subsets is mediated by epinephrine. Int J Sports Med 15(2):100–104PubMedCrossRefGoogle Scholar
  178. Walsh NP, Blannin AK, Clark AM et al (1999) The effects of high-intensity intermittent exercise on saliva IgA, total protein and alpha-amylase. J Sports Sci 17:129–134PubMedCrossRefGoogle Scholar
  179. Walsh NP, Gleeson M, Shephard RJ et al (2011) Position statement. Part one: immune function and exercise. Exerc Immunol Rev 17:6–63PubMedGoogle Scholar
  180. West NP, Pyne DB, Renshaw G et al (2006) Antimicrobial peptides and proteins, exercise and innate mucosal immunity. FEMS Immunol Med Microbiol 48:293–304PubMedCrossRefGoogle Scholar
  181. West NP, Pyne DB, Kyd JM et al (2010) The effect of exercise on innate mucosal immunity. Br J Sports Med 44:227–231PubMedCrossRefGoogle Scholar
  182. Wiggins MS, Simonavice EM (2009) Quality of life benefits in cancer survivorship with supervised exercise. Psychol Rep 104(2):421–424PubMedCrossRefGoogle Scholar
  183. Wilson DO, Johnson P (2000) Exercise modulates antioxidant enzyme gene expression in rat myocardium and liver. J Appl Physiol 88(5):1791–1796PubMedGoogle Scholar
  184. Wood IS, de Heredia FP, Wang B et al (2009) Cellular hypoxia and adipose tissue dysfunction in obesity. Proc Nutr Soc 68:370–377PubMedCrossRefGoogle Scholar
  185. Woods JA, Ceddia MA, Kozak C et al (1997) Effects of exercise on the macrophage MHC II response to inflammation. Int J Sports Med 18:483–488PubMedCrossRefGoogle Scholar
  186. Woods JA, Evans JK, Wolters BW et al (1998) Effects of maximal exercise on natural killer (NK) cell cytotoxicity and responsiveness to interferon-alpha in the young and old. J Gerontol A Biol Sci Med Sci 53:B430–B437PubMedCrossRefGoogle Scholar
  187. Woods JA, Ceddia MA, Wolters BW et al (1999) Effects of 6 months of moderate aerobic exercise training on immune function in the elderly. Mech Ageing Dev 109:1–19PubMedCrossRefGoogle Scholar
  188. World Health Organization (2012) World Health Statistics 2012. http://apps.who.int/iris/bitstream/10665/44844/1/9789241564441_eng.pdf?ua=1&ua=1Assessed. Accessed 7 Jan 2012
  189. Yoda K, Sata T, Kurata T et al (2000) Oropharyngotonsillitis associated with nonprimary Epstein-Barr virus infection. Arch Otolaryngol Head Neck Surg 126:185–193PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Wien 2016

Authors and Affiliations

  1. 1.School of Life, Sport and Social SciencesEdinburgh Napier UniversityEdinburghUK

Personalised recommendations