Advertisement

Asthma in the Athlete

  • Kai-Håkon Carlsen
Part of the Allergy Frontiers book series (ALLERGY, volume 3)

Abstract

Exercise induced asthma (EIA) and bronchial hyperresponsiveness (BHR) have become increasing problems for top athletes within endurance sports. The wide-spread use of asthma drugs among top-athletes has lead the International Olympic Committee, Medical Commission (IOC-MC) and World Anti-Doping Association (WADA) to introduce restriction to the use of asthma drugs in sports.

The present chapter reviews the literature on the prevalence of EIA and BHR among top athletes, discusses the pathogenesis of on one hand EIA, and on the other hand the mechanisms at work for developing asthma and BHR among top athletes.

Asthma is a clinical diagnosis, but may be verified in different ways. The different methods of objectively diagnosis of EIA and BHR among top athletes are described, and possible differential diagnoses to EIA in athletes are discussed. Treatment recommendations for EIA and BHR among athletes are given related to the rules as set up by the IOC-MC and WADA, and the relationship of using asthma drugs related to doping is discussed.

Keywords

Allergy Clin Immunol Elite Athlete Olympic Game Bronchial Hyperresponsiveness Bronchial Responsiveness 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Adams F. The extant works of Aretaeus, the Cappodician. London: The Sydenham Society; 1856.Google Scholar
  2. 2.
    Heir T, Oseid S. Self-reported asthma and exercise-induced asthma symptoms in high-level competitive cross-country skiers. Scand J Med Sci Sports 1994;4:128–33.Google Scholar
  3. 3.
    Larsson K, Ohlsen P, Larsson L, Malmberg P, Rydstrom PO, Ulriksen H. High prevalence of asthma in cross country skiers. BMJ 1993;307(6915):1326–9.PubMedGoogle Scholar
  4. 4.
    Carlsen KH, Oseid S, Odden H, Mellbye E. The response to heavy swimming exercise in children with and without bronchial asthma. In: Oseid S, Carlsen KH (eds) Children and Exercise XIII. Champaign, IL: Human Kinetics Publishers; 1989, pp. 351–60.Google Scholar
  5. 5.
    Helenius IJ, Rytila P, Metso T, Haahtela T, Venge P, Tikkanen HO. Respiratory symptoms, bronchial responsiveness, and cellular characteristics of induced sputum in elite swimmers. Allergy 1998 Apr;53(4):346–52.PubMedCrossRefGoogle Scholar
  6. 6.
    Helenius IJ, Tikkanen HO, Haahtela T. Association between type of training and risk of asthma in elithe athletes. Thorax 1997;52:157–60.PubMedGoogle Scholar
  7. 7.
    Sue-Chue M, Karjalainen EM, Altraja A, Laitinen A, Laitinen LA, Naess AB, et al. Lymphoid aggregates in endobronchial biopsies from young elite cross-country skiers. Am J Respir Crit Care Med 1998;158(2):597–601.Google Scholar
  8. 8.
    Drobnic F, Freixa A, Casan P, Sanchis J, Guardino X. Assessment of chlorine exposure in swimmers during training. Med Sci Sports Exerc 1996;28(2):271–4.PubMedGoogle Scholar
  9. 9.
    Voy RO. The US Olympic Committee experience with exercise-induced bronchospasm, 1984. Med Sci Sports Exerc 1986 June;18(3):328–30.PubMedCrossRefGoogle Scholar
  10. 10.
    Weiler JM, Metzger J, Donnelly AL, Crowley ET, Sharath MD. Prevalence of bronchial responsiveness in highly trained athletes. Chest 1986;90:23–8.PubMedCrossRefGoogle Scholar
  11. 11.
    Weiler JM, Layton T, Hunt M. Asthma in United States Olympic athletes who participated in the 1996 Summer Games. J Allergy Clin Immunol 1998 Nov;102(5):722–6.PubMedCrossRefGoogle Scholar
  12. 12.
    Helbling A, Jenoure P, Muller U. The incidence of hay fever in leading Swiss athletes. Schweiz Med Wochenschr 1990 Feb 17;120(7):231–6.PubMedGoogle Scholar
  13. 13.
    Langdeau JB, Turcotte H, Bowie DM, Jobin J, Desgagne P, Boulet LP. Airway hyperresponsiveness in elite athletes. Am J Respir Crit Care Med 2000 May;161(5):1479–84.PubMedGoogle Scholar
  14. 14.
    Anderson SD, Fitch K, Perry CP, Sue-Chu M, Crapo R, McKenzie D, et al. Responses to bronchial challenge submitted for approval to use inhaled beta2-agonists before an event at the 2002 Winter Olympics. J Allergy Clin Immunol 2003 Jan;111(1):45–50.PubMedCrossRefGoogle Scholar
  15. 15.
    Anderson SD, Sue-Chu M, Perry CP, Gratziou C, Kippelen P, McKenzie DC, et al. Bronchial challenges in athletes applying to inhale a beta2-agonist at the 2004 Summer Olympics. J Allergy Clin Immunol 2006 Apr;117(4):767–73.PubMedCrossRefGoogle Scholar
  16. 16.
    Fitch KD. beta2-Agonists at the Olympic Games. Clin Rev Allergy Immunol 2006 Oct;31(2–3):259–68.PubMedCrossRefGoogle Scholar
  17. 17.
    Heir T, Oseid S. Self-reported asthma and exercise-induced asthma symptoms in high-level competitive cross-country skiers. Scand J Med Sci Sports 1994;4:128–33.Google Scholar
  18. 18.
    Sue-Chu M, Larsson L, Bjermer L. Prevalence of asthma in young cross-country skiers in central Scandinavia: differences between Norway and Sweden. Respir Med 1996 Feb;90(2):99–105.PubMedCrossRefGoogle Scholar
  19. 19.
    Provost-Craig MA, Arbour KS, Sestili DC, Chabalko JJ, Ekinci E. The incidence of exercise-induced bronchospasm in competitive figure skaters. J Asthma 1996;33(1):67–71.PubMedCrossRefGoogle Scholar
  20. 20.
    Mannix ET, Farber MO, Palange P, Galassetti P, Manfredi F. Exercise-induced asthma in figure skaters. Chest 1996;109(2):312–5.PubMedCrossRefGoogle Scholar
  21. 21.
    Rundell KW, Im J, Mayers LB, Wilber RL, Szmedra L, Schmitz HR. Self-reported symptoms and exercise-induced asthma in the elite athlete. Med Sci Sports Exerc 2001 Feb;33(2):208–13.PubMedGoogle Scholar
  22. 22.
    Wilber RL, Rundell KW, Szmedra L, Jenkinson DM, Im J, Drake SD. Incidence of exercise-induced bronchospasm in Olympic winter sport athletes. Med Sci Sports Exerc 2000 Apr;32(4):732–7.PubMedCrossRefGoogle Scholar
  23. 23.
    Feinstein RA, LaRussa J, Wang Dohlman A, Bartolucci AA. Screening adolescent athletes for exercise-induced asthma. Clin J Sport Med 1996;6(2):119–23.PubMedGoogle Scholar
  24. 24.
    Sødal A. Bronchial hyperreactivity, exercise induced asthma and allergy. A study of female national team athletes in soccer. Norwegian University of Sport and Physical Education; 1997.Google Scholar
  25. 25.
    Ross RG. The prevalence of reversible airway obstruction in professional football players. Med Sci Sports Exerc 2000 Dec;32(12):1985–9.PubMedCrossRefGoogle Scholar
  26. 26.
    Schoene RB, Giboney K, Schimmel C, Hagen J, Robinson J, Sato W, et al. Spirometry and airway reactivity in elite track and field athletes. Clin J Sport Med 1997 Oct;7(4):257–61.PubMedCrossRefGoogle Scholar
  27. 27.
    Helenius IJ, Tikkanen HO, Haahtela T. Association between type of training and risk of asthma in elite athletes. Thorax 1997;52:157–60.PubMedCrossRefGoogle Scholar
  28. 28.
    Helenius IJ, Tikkanen HO, Sarna S, Haahtela T. Asthma and increased bronchial responsiveness in elite athletes: atopy and sport event as risk factors. J Allergy Clin Immunol 1998 May;101(5):646–52.PubMedCrossRefGoogle Scholar
  29. 29.
    Maiolo C, Fuso L, Todaro A, Anatra F, Boniello V, Basso S, et al. Prevalence of asthma and atopy in Italian Olympic athletes. Int J Sports Med 2004 Feb;25(2):139–44.PubMedCrossRefGoogle Scholar
  30. 30.
    Nystad W, Harris J, Borgen JS. Asthma and wheezing among Norwegian elite athletes. Med Sci Sports Exerc 2000 Feb;32(2):266–70.PubMedCrossRefGoogle Scholar
  31. 31.
    Dickinson JW, Whyte GP, McConnell AK, Harries MG. Impact of changes in the IOC-MC asthma criteria: a British perspective. Thorax 2005 Aug;60(8):629–32.PubMedCrossRefGoogle Scholar
  32. 32.
    Gilbert IA, McFadden ER, Jr. Airway cooling and rewarming. The second reaction sequence in exercise-induced asthma. J Clin Invest 1992;90:699–704.PubMedCrossRefGoogle Scholar
  33. 33.
    Lee TH, Anderson SD. Heterogeneity of mechanisms in exercise-induced asthma. Thorax 1985;40:481–7.PubMedCrossRefGoogle Scholar
  34. 34.
    Anderson SD. Exercise-induced asthma: Stimulus, mechanism and management. In: Barnes PJ, Roger IW, Thomson NC (eds) Asthma. Basic Mechanisms and Clinical Management. London: Academic; 1988, pp. 503–22.Google Scholar
  35. 35.
    Anderson SD, Daviskas E. The airway microvasculature and exercise induced asthma. Thorax 1992;47:748–52.PubMedCrossRefGoogle Scholar
  36. 36.
    Pauwels R, Joos G, Van der Straten M. Bronchial responsiveness is not bronchial responsiveness is not asthma. Clin Allergy 1988;18:317–21.PubMedCrossRefGoogle Scholar
  37. 37.
    Heir T. Longitudinal variations in bronchial responsiveness in cross-country skiers and control subjects. Scand J Med Sci Sports 1994;4:134–9.CrossRefGoogle Scholar
  38. 38.
    Helenius IJ, Tikkanen HO, Haahtela T. Occurrence of exercise induced bronchospasm in elite runners: dependence on atopy and exposure to cold air and pollen. Br J Sports Med 1998 June;32(2):125–9.PubMedCrossRefGoogle Scholar
  39. 39.
    Heir T, Aanestad G, Carlsen KH, Larsen S. Respiratory tract infection and bronchial responsiveness in elite athletes and sedentary control subjects. Scand J Med Sci Sports 1995;5:94–9.PubMedGoogle Scholar
  40. 40.
    Heir T, Larsen S. The influence of training intensity, airway infections and environmental conditions on seasonal variations in bronchial responsiveness in cross-country skiers. Scand J Med Sci Sports 1995;5:152–9.PubMedGoogle Scholar
  41. 41.
    Sandsund M, Faerevik H, Reinertsen RE, Bjermer L. Effects of breathing cold and warm air on lung function and physical performance in asthmatic and nonasthmatic athletes during exercise in the cold. Ann N Y Acad Sci 1997 Mar 15;813:751–6.PubMedCrossRefGoogle Scholar
  42. 42.
    Drobnic F, Haahtela T. The role of the environment and climate in relation to outdoor and indoor sports. In: Carlsen KH, Delgado L, Del Giacco S (eds) Diagnosis, prevention and treatment of exercise-related asthma, respiratory and allergic disorders in sports. Sheffield, UK: European Respiratory Society Journals Ltd; 2005, pp. 35–47.Google Scholar
  43. 43.
    Bernard A, Carbonnelle S, Michel O, Higuet S, De Burbure C, Buchet JP, et al. Lung hyperpermeability and asthma prevalence in schoolchildren: unexpected associations with the attendance at indoor chlorinated swimming pools. Occup Environ Med 2003 June;60(6):385–94.PubMedCrossRefGoogle Scholar
  44. 44.
    Lagerkvist BJ, Bernard A, Blomberg A, Bergstrom E, Forsberg B, Holmstrom K, et al. Pulmonary epithelial integrity in children: relationship to ambient ozone exposure and swimming pool attendance. Environ Health Perspect 2004 Dec;112(17):1768–71.PubMedGoogle Scholar
  45. 45.
    Nickmilder M, Bernard A. Ecological association between childhood asthma and availability of indoor chlorinated swimming pools in Europe. Occup Environ Med 2007 Jan;64(1):37–46.PubMedCrossRefGoogle Scholar
  46. 46.
    Pierson WE, Covert DS, Koenig JQ, Namekata T, Kim YS. Implications of air pollution effects on athletic performance. Med Sci Sports Exerc 1986 June;18(3):322–7.PubMedCrossRefGoogle Scholar
  47. 47.
    Anderson SD, Silverman M, Tai E, Godfrey S. Specificity of exercise in exercise-induced asthma. Br Med J 1971 Dec 25;4(5790):814–5.PubMedGoogle Scholar
  48. 48.
    Silverman M, Anderson SD. Standardization of exercise tests in asthmatic children. Arch Dis Child 1972 Dec;47(256):882–9.PubMedCrossRefGoogle Scholar
  49. 49.
    Carlsen KH, Engh G, Mørk M. Exercise induced bronchoconstriction depends on exercise load. Respir Med 2000 Aug 2;94:750–5.PubMedCrossRefGoogle Scholar
  50. 50.
    Jonasson G, Carlsen KH, Hultquist C. Low-dose budesonide improves exercise-induced bronchospasm in schoolchildren. Pediatr Allergy Immunol 2000 May;11(2):120–5.PubMedCrossRefGoogle Scholar
  51. 51.
    Carlsen KH, Engh G, Mørk M, Schrøder E. Cold air inhalation and exercise-induced bronchoconstriction in relationship to metacholine bronchial responsiveness. Different patterns in asthmatic children and children with other chronic lung diseases. Respir Med 1998;92(2):308–15.PubMedCrossRefGoogle Scholar
  52. 52.
    Sterk PJ, Fabbri LM, Quanjer PH, Cockcroft DW, O'Byrne PM, Anderson SD, et al. Airway responsiveness. Standardized challenge testing with pharmacological, physical and sensitizing stimuli in adults. Report Working Party Standardization of Lung Function Tests, European Community for Steel and Coal. Official Statement of the European Respiratory Society. Eur Respir J Suppl 1993 Mar;16:53–83.PubMedGoogle Scholar
  53. 53.
    Crapo RO, Casaburi R, Coates AL, Enright PL, Hankinson JL, Irvin CG, et al. Guidelines for methacholine and exercise challenge testing-1999. This official statement of the American Thoracic Society was adopted by the ATS Board of Directors, July 1999. Am J Respir Crit Care Med 2000 Jan;161(1):309–29.PubMedGoogle Scholar
  54. 54.
    Dickinson JW, Whyte GP, McConnell AK, Harries MG. Screening elite winter athletes for exercise induced asthma: a comparison of three challenge methods. Br J Sports Med 2006 Feb;40(2):179–82.PubMedCrossRefGoogle Scholar
  55. 55.
    Mannix ET, Manfredi F, Farber MO. A comparison of two challenge tests for identifying exercise-induced bronchospasm in figure skaters. Chest 1999 Mar;115(3):649–53.PubMedCrossRefGoogle Scholar
  56. 56.
    Slieker MG, van der Ent CK. The diagnostic and screening capacities of peak expiratory flow measurements in the assessment of airway obstruction and bronchodilator response in children with asthma. Monaldi Arch Chest Dis 2003 Apr;59(2):155–9.PubMedGoogle Scholar
  57. 57.
    Quanjer PH, Tammeling GJ, Cotes JE, Pedersen OF, Peslin R, Yernault JC. Lung volumes and forced ventilatory flows. Report Working Party Standardization of Lung Function Tests, European Community for Steel and Coal. Official Statement of the European Respiratory Society. Eur Respir J Suppl 1993 Mar;16:5–40.PubMedGoogle Scholar
  58. 58.
    Anderson SD, Daviskas E. The mechanism of exercise-induced asthma is…. J Allergy Clin Immunol 2000 Sept;106(3):453–9.PubMedCrossRefGoogle Scholar
  59. 59.
    Zach MS, Polgar G. Cold air challenge of airway hyperreactivity in children: dose-response interrelation with a reaction plateau. J Allergy Clin Immunol 1987;80:9–17.PubMedCrossRefGoogle Scholar
  60. 60.
    Anderson SD, Argyros GJ, Magnussen H, Holzer K. Provocation by eucapnic voluntary hyperpnoea to identify exercise induced bronchoconstriction. Br J Sports Med 2001 Oct;35(5):344–7.PubMedCrossRefGoogle Scholar
  61. 61.
    Boulet LP, Legris C, Thibault L, Turcotte H. Comparative bronchial responses to hyperosmolar saline and methacholine in asthma. Thorax 1987 Dec;42(12):953–8.PubMedCrossRefGoogle Scholar
  62. 62.
    Brannan JD, Koskela H, Anderson SD, Chew N. Responsiveness to mannitol in asthmatic subjects with exercise- and hyperventilation-induced asthma. Am J Respir Crit Care Med 1998 Oct;158(4):1120–6.PubMedGoogle Scholar
  63. 63.
    Holzer K, Anderson SD, Chan HK, Douglass J. Mannitol as a challenge test to identify exercise-induced bronchoconstriction in elite athletes. Am J Respir Crit Care Med 2003 Feb 15;167(4):534–7.PubMedCrossRefGoogle Scholar
  64. 64.
    Avital A, Springer C, Bar Yishay E, Godfrey S. Adenosine, methacholine, and exercise challenges in children with asthma or paediatric chronic obstructive pulmonary disease. Thorax 1995;50(5):511–6.PubMedCrossRefGoogle Scholar
  65. 65.
    Godfrey S, Springer C, Noviski N, Maayan Ch, Avital A. Exercise but not metacholine differentiates asthma from chronic lung disease in children. Thorax 1991;46:488–92.PubMedCrossRefGoogle Scholar
  66. 66.
    Koskela HO, Hyvarinen L, Brannan JD, Chan HK, Anderson SD. Sensitivity and validity of three bronchial provocation tests to demonstrate the effect of inhaled corticosteroids in asthma. Chest 2003 Oct;124(4):1341–9.PubMedCrossRefGoogle Scholar
  67. 67.
    Holzer K, Anderson SD, Douglass J. Exercise in elite summer athletes: challenges for diagnosis. J Allergy Clin Immunol 2002 Sept;110(3):374–80.PubMedCrossRefGoogle Scholar
  68. 68.
    Deal ECJ, McFadden ERJ, Ingram RHJ, Jaeger JJ. Hyperpnea and heat flux: initial reaction sequence in exercise-induced asthma. J Appl Physiol 1979 Mar;46(3):476–83.PubMedGoogle Scholar
  69. 69.
    Deal ECJ, McFadden ERJ, Ingram RHJ, Strauss RH, Jaeger JJ. Role of respiratory heat exchange in production of exercise-induced asthma. J Appl Physiol 1979 Mar;46(3):467–75.PubMedGoogle Scholar
  70. 70.
    McFadden ER, Jr., Nelson JA, Skowronski ME, Lenner KA. Thermally induced asthma and airway drying. Am J Respir Crit Care Med 1999 Jul;160(1):221–6.PubMedGoogle Scholar
  71. 71.
    Farley RD, Albazzaz MK, Patel KR. Role of cooling and drying in hyperventilation induced asthma. Thorax 1988 Apr;43(4):289–94.PubMedCrossRefGoogle Scholar
  72. 72.
    Nielsen KG, Bisgaard H. Hyperventilation with cold versus dry air in 2- to 5-year-old children with asthma. Am J Respir Crit Care Med 2005 Feb 1;171(3):238–41.PubMedCrossRefGoogle Scholar
  73. 73.
    Rundell KW, Wilber RL, Szmedra L, Jenkinson DM, Mayers LB, Im J. Exercise-induced asthma screening of elite athletes: field versus laboratory exercise challenge. Med Sci Sports Exerc 2000 Feb;32(2):309–16.PubMedCrossRefGoogle Scholar
  74. 74.
    Rundell KW, Anderson SD, Spiering BA, Judelson DA. Field exercise vs laboratory eucapnic voluntary hyperventilation to identify airway hyperresponsiveness in elite cold weather athletes. Chest 2004 Mar;125(3):909–15.PubMedCrossRefGoogle Scholar
  75. 75.
    Stensrud T, Mykland KV, Gabrielsen K, Carlsen KH. Bronchial hyperresponsiveness in skiers: field test versus methacholine provocation? Med Sci Sports Exerc 2007 Oct;39(10): 1681–6.PubMedCrossRefGoogle Scholar
  76. 76.
    Kotaru C, Coreno A, Skowronski M, Muswick G, Gilkeson RC, McFadden ER, Jr. Morphometric changes after thermal and methacholine bronchoprovocations. J Appl Physiol 2005 Mar;98(3):1028–36.PubMedCrossRefGoogle Scholar
  77. 77.
    Hargreave FE, Ryan G, Thomsom NC, O'Byrne PM, Latimer K, Juniper EF, et al. Bronchial responsiveness to histamine or metacholine in asthma: measurement and clinical significance. J Allergy Clin Immunol 1981;68:347–55.PubMedCrossRefGoogle Scholar
  78. 78.
    Cockcroft DW, Ruffin RE, Dolovich J, Hargreave FE. Allergen-induced increase in non-allergic bronchial reactivity. Clin Allergy 1977;7:503–13.PubMedCrossRefGoogle Scholar
  79. 79.
    Cockcroft DW, Murdock KY, Berscheid BA, Gore BP. Sensitivity and specificity of histamine PC20 determination in a random selection of young college students. J Allergy Clin Immunol 1992 Jan;89(1 Pt 1):23–30.PubMedCrossRefGoogle Scholar
  80. 80.
    Yan K, Salome C, Woolcock AJ. Rapid method for measurement of bronchial responsiveness. Thorax 1983 Oct;38(10):760–5.PubMedCrossRefGoogle Scholar
  81. 81.
    Chinn S, Burney P, Jarvis D, Luczynska C. Variation in bronchial responsiveness in the European Community Respiratory Health Survey (ECRHS). Eur Respir J 1997 Nov;10(11):2495–501.PubMedCrossRefGoogle Scholar
  82. 82.
    Salome CM, Peat JK, Britton J, Woolcock AJ. Bronchial responsiveness in two populations of Australian schoolchildren. I. Relation to respiratory symptoms and diagnosed asthma. Clin Allergy 1987;17:271–81.PubMedCrossRefGoogle Scholar
  83. 83.
    Bonini S, Brusasco V, Carlsen KH, Delgado L, Del Giacco SR, Haahtela T, et al. Diagnosis of asthma and permitted use of inhaled beta2-agonists in athletes. Allergy 2004 Jan;59(1):33–6.PubMedCrossRefGoogle Scholar
  84. 84.
    Landwehr LP, Wood RP, Blager FB, Milgrom H. Vocal cord dysfunction mimicking exercise-induced bronchospasm in adolescents. Pediatrics 1996;98(5):971–4.PubMedGoogle Scholar
  85. 85.
    McFadden ERJ, Zawadski DK. Vocal cord dysfunction masquerading as exercise-induced asthma. a physiologic cause for “choking” during athletic activities. Am J Respir Crit Care Med 1996 Mar;153(3):942–7.PubMedGoogle Scholar
  86. 86.
    Refsum HE, Fønstelien E. Exercise-associated ventilatory insufficiency in adolescent athletes. In: Oseid S, Edwards AM (eds) The asthmatic child in play and sports. London: Pitmann; 1983, pp. 128–39.Google Scholar
  87. 87.
    Heimdal JH, Roksund OD, Halvorsen T, Skadberg BT, Olofsson J. Continuous laryngoscopy exercise test: a method for visualizing laryngeal dysfunction during exercise. Laryngoscope 2006 Jan;116(1):52–7.PubMedCrossRefGoogle Scholar
  88. 88.
    Adir Y, Shupak A, Gil A, Peled N, Keynan Y, Domachevsky L, et al. Swimming-induced pulmonary edema: clinical presentation and serial lung function. Chest 2004 Aug;126(2):394–9.PubMedCrossRefGoogle Scholar
  89. 89.
    Powers SK, Williams J. Exercise-induced hypoxaemia in highly trained athletes. Sports Med 1987 Jan;4(1):46–53.PubMedCrossRefGoogle Scholar
  90. 90.
    Dempsey JA, Johnson BD, Saupe KW. Adaptations and limitations in the pulmonary system during exercise. Chest 1990 Mar;97(3 Suppl):81S–7S.PubMedCrossRefGoogle Scholar
  91. 91.
    Powers SK, Martin D, Cicale M, Collop N, Huang D, Criswell D. Exercise-induced hypoxemia in athletes: role of inadequate hyperventilation. Eur J Appl Physiol Occup Physiol 1992;65(1):37–42.PubMedCrossRefGoogle Scholar
  92. 92.
    Williams JH, Powers SK, Stuart MK. Hemoglobin desaturation in highly trained athletes during heavy exercise. Med Sci Sports Exerc 1986 Apr;18(2):168–73.PubMedGoogle Scholar
  93. 93.
    Durand F, Mucci P, Prefaut C. Evidence for an inadequate hyperventilation inducing arterial hypoxemia at submaximal exercise in all highly trained endurance athletes. Med Sci Sports Exerc 2000 May;32(5):926–32.PubMedCrossRefGoogle Scholar
  94. 94.
    Papalia SM. Aspects of inhaled budesonide use in asthma and exercise Department of Human Movement, University of Western Australia. Thesis; 1996.Google Scholar
  95. 95.
    Henriksen JM, Dahl R. Effects of inhaled budesonide alone and in combination with low-dose terbutaline in children with exercise-induced asthma. Am Rev Respir Dis 1983;128(6):993–7.PubMedGoogle Scholar
  96. 96.
    Meltzer SS, Hasday JD, Cohn J, Bleecker ER. Inhibition of exercise-induced bronchospasm by zileuton: a 5- lipoxygenase inhibitor. Am J Respir Crit Care Med 1996;153(3):931–5.PubMedGoogle Scholar
  97. 97.
    Kemp JP, Dockhorn RJ, Shapiro GG, Nguyen HH, Reiss TF, Seidenberg BC, et al. Montelukast once daily inhibits exercise-induced bronchoconstriction in 6- to 14-year-old children with asthma. J Pediatr 1998 Sep;133(3):424–8.PubMedCrossRefGoogle Scholar
  98. 98.
    Leff JA, Busse WW, Pearlman D, Bronsky E, Kemp J, Hendeles L, et al. Montelukast, a leukotriene-receptor antagonist, for the treatment of mild asthma and exercise-induced bronchoconstriction. N Engl J Med 1998;339:147–52.PubMedCrossRefGoogle Scholar
  99. 99.
    Villaran C, O'Neill SJ, Helbling A, Van Noord JA, Lee TH, Chuchalin AG, et al. Montelukast versus salmeterol in patients with asthma and exercise- induced bronchoconstriction. J Allergy Clin Immunol 1999 Sept;104(3 Pt 1):547–53.PubMedCrossRefGoogle Scholar
  100. 100.
    de Benedictis FM, del Giudice MM, Forenza N, Decimo F, de BD, Capristo A. Lack of tolerance to the protective effect of montelukast in exercise-induced bronchoconstriction in children. Eur Respir J 2006 Aug;28(2):291–5.PubMedCrossRefGoogle Scholar
  101. 101.
    Freeman W, Williams C, Nute MG. Endurance running performance in athletes with asthma. J Sports Sci 1990;8(2):103–17.PubMedGoogle Scholar
  102. 102.
    Carlsen KH, Larsson K. The efficacy of inhaled disodium cromoglycate and glucocorticoids. Clin Exp Allergy 1996;26(Suppl 4):8–17.PubMedCrossRefGoogle Scholar
  103. 103.
    Benedictis FM, Tuteri G, Bertotto A, Bruni L, Vaccaro R. Comparison of the protective effects of cromolyn sodium and nedocromil sodium in the treatment of exercise-induced asthma in children. J Allergy Clin Immunol 1994;94:684–8.PubMedCrossRefGoogle Scholar
  104. 104.
    Woolley M, Anderson SD, Quigley BM. Duration of protective effect of terbutaline sulfate and cromolyn sodium alone and in combination on exercise-induced asthma. Chest 1990;97:39–45.PubMedCrossRefGoogle Scholar
  105. 105.
    Anderson SD. Drugs and the control of exercise-induced asthma [editorial; comment]. Eur Respir J 1993;6:1090–2.PubMedGoogle Scholar
  106. 106.
    Green CP, Price JF. Prevention of exercise induced asthma by inhaled salmeterol xinafoate. Arch Dis Child 1992;67:1014–7.PubMedCrossRefGoogle Scholar
  107. 107.
    Steffensen I, Faurschou P, Riska H, Rostrup J, Wegener T. Inhaled formoterol dry powder in the treatment of patients with reversible obstructive airway disease. A 3-month, placebo- controlled comparison of the efficacy and safety of formoterol and salbutamol, followed by a 12-month trial with formoterol. Allergy 1995;50(8):657–63.PubMedCrossRefGoogle Scholar
  108. 108.
    De Lepeleire I, Reiss TF, Rochette F, Botto A, Zhang J, Kundu S, et al. Montelukast causes prolonged, potent leukotriene D4-receptor antagonism in the airways of patients with asthma. Clin Pharmacol Ther 1997 Jan;61(1):83–92.PubMedCrossRefGoogle Scholar
  109. 109.
    Lynch GS, Hayes A, Campbell SP, Williams DA. Effects of beta 2-agonist administration and exercise on contractile activation of skeletal muscle fibers. J Appl Physiol 1996 Oct;81(4):1610–8.PubMedGoogle Scholar
  110. 110.
    Dodd SL, Powers SK, Vrabas IS, Criswell D, Stetson S, Hussain R. Effects of clenbuterol on contractile and biochemical properties of skeletal muscle. Med Sci Sports Exerc 1996 June;28(6):669–76.PubMedGoogle Scholar
  111. 111.
    Suzuki J, Gao M, Xie Z, Koyama T. Effects of the beta(2)-adrenergic agonist clenbuterol on capillary geometry in cardiac and skeletal muscles in young and middle-aged rats. Acta Physiologica Scandinavica 1997 Nov;161(3):317–26.PubMedCrossRefGoogle Scholar
  112. 112.
    Hayes A, Williams DA. Contractile properties of clenbuterol-treated mdx muscle are enhanced by low-intensity swimming. J Appl Physiol 1997 Feb;82(2):435–9.PubMedGoogle Scholar
  113. 113.
    Lynch GS, Hayes A, Campbell SP, Williams DA. Effects of beta 2-agonist administration and exercise on contractile activation of skeletal muscle fibers. J Appl Physiol 1996 Oct;81(4):1610–8.PubMedGoogle Scholar
  114. 114.
    Duncan ND, Williams DA, Lynch GS. Deleterious effects of chronic clenbuterol treatment on endurance and sprint exercise performance in rats. Clin Sci (Lond) 2000 Mar;98(3):339–47.CrossRefGoogle Scholar
  115. 115.
    Van Der Heijden HF, Zhan WZ, Prakash YS, Dekhuijzen PN, Sieck GC. Salbutamol enhances isotonic contractile properties of rat diaphragm muscle. J Appl Physiol 1998 Aug;85(2):525–9.Google Scholar
  116. 116.
    Buchanan R, Nielsen OB, Clausen T. Excitation- and beta(2)-agonist-induced activation of the Na(+)-K(+) pump in rat soleus muscle. J Physiol 2002 Nov 15;545(Pt 1):229–40.PubMedCrossRefGoogle Scholar
  117. 117.
    Caruso JF, Signorile JF, Perry AC, Leblanc B, Williams R, Clark M, et al. The effects of albuterol and isokinetic exercise on the quadriceps muscle group. Med Sci Sports Exerc 1995 Nov;27(11):1471–6.PubMedGoogle Scholar
  118. 118.
    van Baak MA, Mayer LH, Kempinski RE, Hartgens F. Effect of salbutamol on muscle strength and endurance performance in nonasthmatic men. Med Sci Sports Exerc 2000 Jul;32(7):1300–6.PubMedCrossRefGoogle Scholar
  119. 119.
    Violante B, Pellegrino R, Vinay C, Selleri R, Ghinamo G. Failure of aminophylline and salbutamol to improve respiratory muscle function and exercise tolerance in healthy humans. Respiration 1989;55(4):227–36.PubMedCrossRefGoogle Scholar
  120. 120.
    Javaheri S, Smith JT, Thomas JP, Guilfoile TD, Donovan EF. Albuterol has no effect on diaphragmatic fatigue in humans. Am Rev Respir Dis 1988 Jan;137(1):197–201.PubMedGoogle Scholar
  121. 121.
    Lanigan C, Howes TQ, Borzone G, Vianna LG, Moxham J. The effects of beta 2-agonists and caffeine on respiratory and limb muscle performance. Eur Respir J 1993 Sep;6(8):1192–6.PubMedGoogle Scholar
  122. 122.
    Collomp K, Candau R, Collomp R, Carra J, Lasne F, Prefaut C, et al. Effects of acute ingestion of salbutamol during submaximal exercise. Int J Sports Med 2000 Oct;21(7):480–4.PubMedCrossRefGoogle Scholar
  123. 123.
    Meeuwisse WH, McKenzie DC, Hopkins S, Road JD, Hopkins SR. The effect of salbutamol on performance in nonasthmatic athletes. Med Sci Sports Exerc 1992;24:1161–6.PubMedGoogle Scholar
  124. 124.
    Morton AR, Papalia SM, Fitch KD. Changes in anaerobic power and strength performance after inhalation of salbutamol in nonasthmatic athletes. Clin J Sport Med 1993;3:14–9.CrossRefGoogle Scholar
  125. 125.
    Lemmer JT, Fleck SJ, Wallach JM, Fox S, Burke ER, Kearney JT, et al. The effects of albuterol on power output in non-asthmatic athletes. Int J Sports Med 1995 May;16(4):243–9.PubMedCrossRefGoogle Scholar
  126. 126.
    Morton AR, Joyce K, Papalia SM, Carroll NG, Fitch KD. Is salmeterol ergogenic? Clin J Sport Med 1996;6(4):220–5.PubMedCrossRefGoogle Scholar
  127. 127.
    McDowell SL, Fleck SJ, Storms WW. The effects of salmeterol on power output in nonasthmatic athletes. J Allergy Clin Immunol 1997 Apr;99(4):443–9.PubMedCrossRefGoogle Scholar
  128. 128.
    Signorile JF, Kaplan TA, Applegate B, Perry AC. Effects of acute inhalation of the bronchodilator, albuterol, on power output. Med Sci Sports Exerc 1992;24:638–42.PubMedGoogle Scholar
  129. 129.
    Morton AR, Papalia SM, Fitch KD. Is salbutamol ergogenic?: the effects of salbutamol on physical performance in the high-performance nonasthmatic athletes. Clin J Sport Med 1992;2:93–7.CrossRefGoogle Scholar
  130. 130.
    Meeuwisse WH, McKenzie DC, Hopkins SR, Road JD. The effect of salbutamol on performance in elite nonasthmatic athletes. Med Sci Sports Exerc 1992 Oct;24(10):1161–6.PubMedGoogle Scholar
  131. 131.
    Fleck SJ, Lucia A, Storms WW, Wallach JM, Vint PF, Zimmerman SD. Effects of acute inhalation of albuterol on submaximal and maximal VO2 and blood lactate. Int J Sports Med 1993 July;14(5):239–43.PubMedCrossRefGoogle Scholar
  132. 132.
    Heir T, Stemshaug H. Sabutamol and high-intensity treadmill running in nonasthmatic highly conditioned athletes. Scand J Med Sci Sports 1995;5:231–6.PubMedCrossRefGoogle Scholar
  133. 133.
    Unnithan VB, Thomson KJ, Aitchison TC, Paton JY. β2-Agonists and Running Economy in Prepubertal Boys. Pediatr Pulmonol 1994;17:378–82.PubMedCrossRefGoogle Scholar
  134. 134.
    Goubault C, Perault MC, Leleu E, Bouquet S, Legros P, Vandel B, et al. Effects of inhaled salbutamol in exercising non-asthmatic athletes. Thorax 2001 Sept;56(9):675–9.PubMedCrossRefGoogle Scholar
  135. 135.
    Carlsen KH, Ingjer F, Thyness B, Kirkegaard H. The effect of inhaled salbutamol and salmeterol on lung function and endurance performance in healthy well-trained athletes. Scand J Med Sci Sports 1997;7:160–5.PubMedCrossRefGoogle Scholar
  136. 136.
    Sue-Chu M, Sandsund M, Helgerud J, Reinertsen RE, Bjermer L. Salmeterol and physical performance at -15 degrees C in highly trained nonasthmatic cross-country skiers. Scand J Med Sci Sports 1999 Feb;9(1):48–52.PubMedCrossRefGoogle Scholar
  137. 137.
    Carlsen KH, Hem E, Stensrud T, Held T, Herland K, Mowinckel P. Can asthma treatment in sports be doping? The effect of the rapid onset, long-acting inhaled β2-agonist formoterol upon endurance performance in healthy well-trained athletes. Respir Med 2001 July;95(7):571–6.PubMedCrossRefGoogle Scholar
  138. 138.
    Stewart IB, Labreche JM, McKenzie DC. Acute formoterol administration has no ergogenic effect in nonasthmatic athletes. Med Sci Sports Exerc 2002 Feb;34(2):213–7.PubMedCrossRefGoogle Scholar
  139. 139.
    Riiser A, Tjorhom A, Carlsen KH. The effect of formoterol inhalation on endurance performance in hypobaric conditions. Med Sci Sports Exerc 2006 Dec;38(12):2132–7.PubMedCrossRefGoogle Scholar
  140. 140.
    Tjorhom A, Riiser A, Carlsen KH. Effects of formoterol on endurance performance in athletes at an ambient temperature of -20 degrees C. Scand J Med Sci Sports 2007 Feb 19.Google Scholar
  141. 141.
    Sue-Chu M, Sandsund M, Holand B, Bjermer L. Montelukast does not affect exercise performance at subfreezing temperature in highly trained non-asthmatic endurance athletes [In Process Citation]. Int J Sports Med 2000 Aug;21(6):424–8.PubMedCrossRefGoogle Scholar

Copyright information

© Springer 2009

Authors and Affiliations

  • Kai-Håkon Carlsen
    • 1
  1. 1.VoksentoppenOsloNorway

Personalised recommendations