Exercise, immune function and respiratory infection: An update on the influence of training and environmental stress

Immunology and Cell Biology

Volumn 94, Issue 2, 2016, Pages 132-139

  Walsh, Neil P ^a   Oliver, Samuel J ^a  

^a BANGOR UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTIVE IMMUNITY; ALTITUDE; ENVIRONMENTAL STRESS; EXERCISE; HUMAN; IMMUNE SYSTEM; IMMUNITY; INNATE IMMUNITY; REVIEW; TEMPERATURE STRESS; UPPER RESPIRATORY TRACT INFECTION; ADVERSE EFFECTS; ANIMAL; ATHLETE; ATHLETIC PERFORMANCE; ENVIRONMENTAL EXPOSURE; GENETIC PREDISPOSITION; GENETICS; IMMUNOLOGY; IMMUNOSUPPRESSIVE TREATMENT; PHYSIOLOGICAL STRESS; PHYSIOLOGY; RESPIRATORY TRACT INFECTION;

ANIMALS; ATHLETES; ATHLETIC PERFORMANCE; ENVIRONMENTAL EXPOSURE; EXERCISE; GENETIC PREDISPOSITION TO DISEASE; HUMANS; IMMUNITY; IMMUNOSUPPRESSION; PHYSICAL EXERTION; RESPIRATORY TRACT INFECTIONS; STRESS, PHYSIOLOGICAL;

EID: 84983134090     PISSN: 08189641     EISSN: 14401711     Source Type: Journal    
DOI: 10.1038/icb.2015.99     Document Type: Review

References (94)

1. Nieman DC, Johanssen LM, Lee JW, Arabatzis K. Infectious episodes in runners before and after the Los Angeles Marathon. J Sports Med Phys Fitness 1990; 30: 316-328.
2. Peters EM, Bateman ED. Ultramarathon running and upper respiratory tract infections. An epidemiological survey. S Afr Med J 1983; 64: 582-584.
3. Tomasi TB, Trudeau FB, Czerwinski D, Erredge S. Immune parameters in athletes before and after strenuous exercise. J Clin Immunol 1982; 2: 173-178.
4. Keast D, Cameron K, Morton AR. Exercise and the immune response. Sports Med 1988; 5: 248-267.
5. Fitzgerald L. Exercise and the immune system. Immunol Today 1988; 9: 337-339.
6. Walsh NP, Gleeson M, Shephard RJ, Gleeson M, Woods JA, Bishop NC et al. Position statement. Part one: Immune function and exercise. Exerc Immunol Rev 2011; 17: 6-63.
7. Walsh NP, Gleeson M, Pyne DB, Nieman DC, Dhabhar FS, Shephard RJ et al. Position statement. Part two: Maintaining immune health. Exerc Immunol Rev 2011; 17: 64-103.
8. Shephard RJ. Immune changes induced by exercise in an adverse environment. Can J Physiol Pharmacol 1998; 76: 539-546.
9. Spence L, Brown WJ, Pyne DB, Nissen MD, Sloots TP, McCormack JG et al. Incidence, etiology, and symptomatology of upper respiratory illness in elite athletes. Med Sci Sports Exerc 2007; 39: 577-586.
10. Martensson S, Nordebo K, Malm C. High training volumes are associated with a low number of self-reported sick days in elite endurance athletes. J Sports Sci Med 2014; 13: 929-933.
11. Hellard P, Avalos M, Guimaraes F, Toussaint JF, Pyne DB. Training-related risk of common illnesses in elite swimmers over a 4-yr period. Med Sci Sports Exerc 2015; 47: 698-707.
12. Fondell E, Lagerros YT, Sundberg CJ, Lekander M, Balter O, Rothman KJ et al. Physical activity, stress, and self-reported upper respiratory tract infection. Med Sci Sports Exerc 2011; 43: 272-279.
13. Nieman DC. Exercise, upper respiratory tract infection, and the immune system. Med Sci Sports Exerc 1994; 26: 128-139.
14. Trammell RA, Toth LA. Genetic susceptibility and resistance to influenza infection and disease in humans and mice. Expert Rev Mol Diagn 2008; 8: 515-529.
15. Shin DL, Hatesuer B, Bergmann S, Nedelko T, Schughart K. Protection from severe influenza virus infections in mice carrying the Mx1 influenza virus resistance gene strongly depends on genetic background. J Virol 2015; 89: 9998-10009.
16. Everitt AR, Clare S, Pertel T, John SP, Wash RS, Smith SE et al. IFITM3 restricts the morbidity and mortality associated with influenza. Nature 2012; 484: 519-523.
17. Cox AJ, Gleeson M, Pyne DB, Callister R, Hopkins WG, Fricker PA. Clinical and laboratory evaluation of upper respiratory symptoms in elite athletes. Clin J Sport Med 2008; 18: 438-445.
18. Robson-Ansley P, Howatson G, Tallent J, Mitcheson K, Walshe I, Toms C et al. Prevalence of allergy and upper respiratory tract symptoms in runners of the London marathon. Med Sci Sports Exerc 2012; 44: 999-1004.
19. Arruda E, Pitkaranta A, Witek TJ Jr, Doyle CA, Hayden FG. Frequency and natural history of rhinovirus infections in adults during autumn. J Clin Microbiol 1997; 35: 2864-2868.
20. He CS, Handzlik M, Muhamad A, Gleeson M. Influence of CMV/EBV serostatus on respiratory infection incidence during 4 months of winter training in a student cohort of endurance athletes. Eur J Appl Physiol 2013; 113: 2613-2619.
21. Pyne DB, Hopkins WG, Batterham AM, Gleeson M, Fricker PA. Characterising the individual performance responses to mild illness in international swimmers. Br J Sports Med 2005; 39: 752-756.
22. Dhabhar FS. Effects of stress on immune function: the good, the bad, and the beautiful. Immunol Res 2014; 58: 193-210.
23. Nieman DC, Luo B, Dreau D, Henson DA, Shanely RA, Dew D et al. Immune and inflammation responses to a 3-day period of intensified running versus cycling. Brain Behav Immun 2014; 39: 180-185.
24. Suchanek O, Podrazil M, Fischerova B, Bocinska H, Budinsky V, Stejskal D et al. Intensive physical activity increases peripheral blood dendritic cells. Cell Immunol 2010; 266: 40-45.
25. LaVoy EC, Bollard CM, Hanley PJ, O'Connor DP, Lowder TW, Bosch JA et al. A single bout of dynamic exercise by healthy adults enhances the generation of monocyte-derived-dendritic cells. Cell Immunol 2015; 295: 52-59.
26. Simpson RJ. Aging, persistent viral infections, and immunosenescence: can exercise 'make space' Exerc Sport Sci Rev 2011; 39: 23-33.
27. Prieto-Hinojosa A, Knight A, Compton C, Gleeson M, Travers PJ. Reduced thymic output in elite athletes. Brain Behav Immun 2014; 39: 75-79.
28. Witard OC, Turner JE, Jackman SR, Tipton KD, Jeukendrup AE, Kies AK et al. High-intensity training reduces CD8+ T-cell redistribution in response to exercise. Med Sci Sports Exerc 2012; 44: 1689-1697.
29. Brown FF, Bigley AB, Sherry C, Neal CM, Witard OC, Simpson RJ et al. Training status and sex influence on senescent T-lymphocyte redistribution in response to acute maximal exercise. Brain Behav Immun 2014; 39: 152-159.
30. Gleeson M, Bishop N, Oliveira M, McCauley T, Tauler P. Sex differences in immune variables and respiratory infection incidence in an athletic population. Exerc Immunol Rev 2011; 17: 122-135.
31. Handzlik MK, Shaw AJ, Dungey M, Bishop NC, Gleeson M. The influence of exercise training status on antigen-stimulated IL-10 production in whole blood culture and numbers of circulating regulatory T cells. Eur J Appl Physiol 2013; 113: 1839-1848.
32. Gleeson M, Bishop N, Oliveira M, Tauler P. Influence of training load on upper respiratory tract infection incidence and antigen-stimulated cytokine production. Scand J Med Sci Sports 2013; 23: 451-457.
33. Diment BC, Fortes MB, Edwards JP, Hanstock HG, Ward MD, Dunstall HM et al. Exercise intensity and duration effects on in vivo immunity. Med Sci Sports Exerc 2015; 47: 1390-1398.
34. Pascoe AR, Fiatarone Singh MA, Edwards KM. The effects of exercise on vaccination responses: a review of chronic and acute exercise interventions in humans. Brain Behav Immun 2014; 39: 33-41.
35. Harper Smith AD, Coakley SL, Ward MD, Macfarlane AW, Friedmann PS, Walsh NP. Exercise-induced stress inhibits both the induction and elicitation phases of in vivo T-cell-mediated immune responses in humans. Brain Behav Immun 2011; 25: 1136-1142.
36. Levine BD, Stray-Gundersen J, Mehta RD. Effect of altitude on football performance. Scand J Med Sci Sports 2008; 18 (Suppl 1): 76-84.
37. Racinais S, Alonso JM, Coutts AJ, Flouris AD, Girard O, Gonzalez-Alonso J et al. Consensus recommendations on training and competing in the heat. Br J Sports Med 2015; 49: 1164-1173.
38. Wilder-Smith A, Mustafa FB, Peng CM, Earnest A, Koh D, Lin G et al. Transient immune impairment after a simulated long-haul flight. Aviat Space Environ Med 2012; 83: 418-423.
39. Galloway SD, Maughan RJ. Effects of ambient temperature on the capacity to perform prolonged cycle exercise in man. Med Sci Sports Exerc 1997; 29: 1240-1249.
40. Walsh NP, Whitham M. Exercising in environmental extremes: a greater threat to immune function Sports Med 2006; 36: 941-976.
41. Severs Y, Brenner I, Shek PN, Shephard RJ. Effects of heat and intermittent exercise on leukocyte and sub-population cell counts. Eur J Appl Physiol Occup Physiol 1996; 74: 234-245.
42. Castellani JW, Brenner IKM, Rhind SG. Cold exposure: human immune responses and intracellular cytokine expression. Med Sci Sports Exerc 2002; 34: 2013-2020.
43. Maresh CM, Whittlesey MJ, Armstrong LE, Yamamoto LM, Judelson DA, Fish KE et al. Effect of hydration state on testosterone and cortisol responses to training-intensity exercise in collegiate runners. Int J Sports Med 2006; 27: 765-770.
44. Fortes MB, Diment BC, Di Felice U, Walsh NP. Dehydration decreases saliva antimicrobial proteins important for mucosal immunity. Appl Physiol Nutr Metab 2012; 37: 850-859.
45. Hanstock HG, Walsh NP, Edwards JP, Fortes MB, Cosby SL, Nugent A et al. Tear fluid SIgA as a noninvasive biomarker of mucosal immunity and common cold risk. Med Sci Sports Exerc (e-pub ahead of print 22 October 2015; doi:10.1249/MSS.0000000000000801).
46. Killer SC, Svendsen IS, Gleeson M. The influence of hydration status during prolonged endurance exercise on salivary antimicrobial proteins. Eur J Appl Physiol 2015; 115: 1887-1895.
47. Svendsen IS, Killer SC, Gleeson M. Influence of hydration status on changes in plasma cortisol, leukocytes, and antigen-stimulated cytokine production by whole blood culture following prolonged exercise. ISRN Nutr 2014; 2014: 561401.
48. Wall BA, Watson G, Peiffer JJ, Abbiss CR, Siegel R, Laursen PB. Current hydration guidelines are erroneous: dehydration does not impair exercise performance in the heat. Br J Sports Med 2015; 49: 1077-1083.
49. Dokladny K, Zuhl MN, Moseley PL. Intestinal epithelial barrier function and tight junction proteins with heat and exercise. J Appl Physiol (e-pub ahead of print 10 September 2015; doi:10.1152/japplphysiol.00536.2015).
50. Fortes MB, Di Felice U, Dolci A, Junglee NA, Crockford MJ, West L et al. Muscle-damaging exercise increases heat strain during subsequent exercise heat stress. Med Sci Sports Exerc 2013; 45: 1915-1924.
51. Kuennen M, Gillum T, Dokladny K, Bedrick E, Schneider S, Moseley P. Thermotolerance and heat acclimation may share a common mechanism in humans. Am J Physiol Regul Integr Comp Physiol 2011; 301: R524-R533.
52. Ernst E, Pecho E, Wirz P, Saradeth T. Regular sauna bathing and the incidence of common colds. Ann Med 1990; 22: 225-227.
53. Makinen TM, Juvonen R, Jokelainen J, Harju TH, Peitso A, Bloigu A et al. Cold temperature and low humidity are associated with increased occurrence of respiratory tract infections. Respir Med 2009; 103: 456-462.
54. Eccles R, Wilkinson JE. Exposure to cold and acute upper respiratory tract infection. Rhinology 2015; 53: 99-106.
55. Jansky L, Pospisilova D, Honzova S, Ulicny B, Sramek P, Zeman V et al. Immune system of cold-exposed and cold-adapted humans. Eur J Appl Physiol Occup Physiol 1996; 72: 445-450.
56. Roberts LA, Raastad T, Markworth JF, Figueiredo VC, Egner IM, Shield A et al. Post-exercise cold water immersion attenuates acute anabolic signalling and long-term adaptations in muscle to strength training. J Physiol 2015; 593: 4285-4301.
57. Millet GP, Faiss R, Brocherie F, Girard O. Hypoxic training and team sports: a challenge to traditional methods Br J Sports Med 2013; 47 (Suppl 1): 16-17.
58. Lundby C, Millet GP, Calbet JA, Bartsch P, Subudhi AW. Does 'altitude training' increase exercise performance in elite athletes Br J Sports Med 2012; 46: 792-795.
59. Gore CJ, Hahn A, Rice A, Bourdon P, Lawrence S, Walsh C et al. Altitude training at 2690m does not increase total haemoglobin mass or sea level VO2max in world champion track cyclists. J Sci Med Sport 1998; 1: 156-170.
60. Bailey DM, Davies B, Romer L, Castell L, Newsholme E, Gandy G. Implications of moderate altitude training for sea-level endurance in elite distance runners. Eur J Appl Physiol Occup Physiol 1998; 78: 360-368.
61. Zhang Y, Hu Y, Wang F. Effects of a 28-day 'living high-training low' on T-lymphocyte subsets in soccer players. Int J Sports Med 2007; 28: 354-358.
62. Oliver SJ, Macdonald JH, Harper Smith AD, Lawley JS, Gallagher CA, Di Felice U et al. High altitude impairs in vivo immunity in humans. High Alt Med Biol 2013; 14: 144-149.
63. Oliver SJ, Sanders SJ, Williams CJ, Smith ZA, Lloyd-Davies E, Roberts R et al. Physiological and psychological illness symptoms at high altitude and their relationship with acute mountain sickness: a prospective cohort study. J Travel Med 2012; 19: 210-219.
64. Pyne DB, McDonald WA, Morton DS, Swiggett JP, Foster M, Sonnenfeld G et al. Inhibition of interferon, cytokine, and lymphocyte proliferative responses in elite swimmers with altitude exposure. J Interf Cytok Res 2000; 20: 411-418.
65. Wang JS, Lin CT. Systemic hypoxia promotes lymphocyte apoptosis induced by oxidative stress during moderate exercise. Eur J Appl Physiol 2010; 108: 371-382.
66. Facco M, Zilli C, Siviero M, Ermolao A, Travain G, Baesso I et al. Modulation of immune response by the acute and chronic exposure to high altitude. Med Sci Sport Exerc 2005; 37: 768-774.
67. Hitomi Y, Miyamura M, Mori S, Suzuki K, Kizaki T, Itoh C et al. Intermittent hypobaric hypoxia increases the ability of neutrophils to generate superoxide anion in humans. Clin Exp Pharmacol Physiol 2003; 30: 659-664.
68. Wang JS, Chen WL, Weng TP. Hypoxic exercise training reduces senescent T-lymphocyte subsets in blood. Brain Behav Immun 2011; 25: 270-278.
69. Born DP, Faiss R, Willis SJ, Strahler J, Millet GP, Holmberg HC et al. Circadian variation of salivary immunoglobin A, alpha-amylase activity and mood in response to repeated double-poling sprints in hypoxia. Eur J Appl Physiol (e-pub ahead of print 3 August 2015; doi:10.1007/s00421-015-3236-3).
70. Lovallo WR. Do low levels of stress reactivity signal poor states of health Biol Psychol 2011; 86: 121-128.
71. Bosch JA, Ring C, de Geus EJ, Veerman EC, Amerongen AV. Stress and secretory immunity. Int Rev Neurobiol 2002; 52: 213-253.
72. Brenner IKM, Severs YD, Shek PN, Shephard RJ. Impact of heat exposure and moderate, intermittent exercise on cytolytic cells. Eur J Appl Physiol Occup Physiol 1996; 74: 162-171.
73. Peake J, Peiffer JJ, Abbiss CR, Nosaka K, Okutsu M, Laursen PB et al. Body temperature and its effect on leukocyte mobilization, cytokines and markers of neutrophil activation during and after exercise. Eur J Appl Physiol 2008; 102: 391-401.
74. McFarlin BK, Mitchell JB. Exercise in hot and cold environments: differential effects on leukocyte number and NK cell activity. Aviat Space Environ Med 2003; 74: 1231-1236.
75. Mitchell JB, Dugas JP, McFarlin BK, Nelson MJ. Effect of exercise, heat stress, and hydration on immune cell number and function. Med Sci Sports Exerc 2002; 34: 1941-1950.
76. Brenner IK, Castellani JW, Gabaree C, Young AJ, Zamecnik J, Shephard RJ et al. Immune changes in humans during cold exposure: effects of prior heating and exercise. J Appl Physiol 1999; 87: 699-710.
77. Lackovic V, Borecky L, Vigas M, Rovensky J. Activation of NK cells in subjects exposed to mild hyper-or hypothermic load. J Interferon Res 1988; 8: 393-402.
78. Meehan R, Duncan U, Neale L, Taylor G, Muchmore H, Scott N et al. Operation Everest II: alterations in the immune system at high altitudes. J Clin Immunol 1988; 8: 397-406.
79. Klokker M, Kjaer M, Secher NH, Hanel B, Worm L, Kappel M et al. Natural-Killer-Cell Response to Exercise in Humans-Effect of Hypoxia and Epidural-Anesthesia. J Appl Physiol 1995; 78: 709-716.
80. Wang JS, Wu CK. Systemic hypoxia affects exercise-mediated antitumor cytotoxicity of natural killer cells. J Appl Physiol 2009; 107: 1817-1824.
81. Laing SJ, Blackwell J, Gwynne D, Walters R, Walsh NP. Neutrophil degranulation response to 2 hours of exercise in a 30 degrees C environment. Aviat Space Environ Med 2005; 76: 1068-1073.
82. Laing SJ, Oliver SJ, Wilson S, Walters R, Bilzon JL, Walsh NP. Neutrophil-degranulation and lymphocyte-subset response after 48 hr of fluid and/or energy restriction. Int J Sport Nutr Exerc Metab 2008; 18: 443-456.
83. Costa RJ, Smith AH, Oliver SJ, Walters R, Maassen N, Bilzon JL et al. The effects of two nights of sleep deprivation with or without energy restriction on immune indices at rest and in response to cold exposure. Eur J Appl Physiol 2010; 109: 417-428.
84. Wang JS, Chiu YT. Systemic hypoxia enhances exercise-mediated bactericidal and subsequent apoptotic responses in human neutrophils. J Appl Physiol 2009; 107: 1213-1222.
85. Chouker A, Demetz F, Martignoni A, Smith L, Setzer F, Bauer A et al. Strenuous physical exercise inhibits granulocyte activation induced by high altitude. J Appl Physiol 2005; 98: 640-647.
86. Laing SJ, Gwynne D, Blackwell J, Williams M, Walters R, Walsh NP. Salivary IgA response to prolonged exercise in a hot environment in trained cyclists. Eur J Appl Physiol 2005; 93: 665-671.
87. Ermolao A, Travain G, Facco M, Zilli C, Agostini C, Zaccaria M. Relationship between stress hormones and immune response during high-altitude exposure in women. J Endocrinol Invest 2009; 32: 889-894.
88. Biselli R, Le Moli S, Matricardi PM, Farrace S, Fattorossi A, Nisini R et al. The effects of hypobaric hypoxia on specific B cell responses following immunization in mice and humans. Aviat Space Environ Med 1991; 62: 870-874.
89. Sawka MN, Young AJ, Dennis RC, Gonzalez RR, Pandolf KB, Valeri CR. Human intravascular immunoglobulin responses to exercise-heat and hypohydration. Aviat Space Environ Med 1989; 60: 634-638.
90. Kleessen B, Schroedl W, Stueck M, Richter A, Rieck O, Krueger M. Microbial and immunological responses relative to high-altitude exposure in mountaineers. Med Sci Sports Exerc 2005; 37: 1313-1318.
91. Coste O, Van Beers P, Bogdan A, Touitou Y. Human immune circadian system in prolonged mild hypoxia during simulated flights. Chronobiol Int 2007; 24: 87-98.
92. Oliver SJ, Laing SJ, Wilson S, Bilzon JL, Walters R, Walsh NP. Salivary immunoglobulin A response at rest and after exercise following a 48 h period of fluid and/or energy restriction. Br J Nutr 2007; 97: 1109-1116.
93. Walsh NP, Bishop NC, Blackwell J, Wierzbicki SG, Montague JC. Salivary IgA response to prolonged exercise in a cold environment in trained cyclists. Med Sci Sports Exerc 2002; 34: 1632-1637.
94. Tiollier E, Schmitt L, Burnat P, Fouillot JP, Robach P, Filaire E et al. Living high-training low altitude training: effects on mucosal immunity. Eur J Appl Physiol 2005; 94: 298-304.