Mechanisms and Management of Exercise-Induced Asthma in Elite Athletes

References

• Stenfors N. Self-reported symptoms and bronchial hyperresponsiveness in elite cross-country skiers. Respir Med. 2010; 104:1760–1763.
   PubMed Web of Science ®Google Scholar
• 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; 33:208–213.
   PubMed Web of Science ®Google Scholar
• Hallstrand TS, Curtis JR, Koepsell TD, Martin DP, Schoene RB, Sullivan SD. Effectiveness of screening examinations to detect unrecognized exercise-induced bronchoconstriction. J Pediatr. 2002; 141:343–348.
   PubMed Web of Science ®Google Scholar
• Larsson K, Ohlsen P, Larsson L, Malmberg P, Rydstrøm PO, Ulriksen H. High prevalence of asthma in cross country skiers. BMJ 1993; 307:1326–1329.
   PubMed Web of Science ®Google Scholar
• Weiler JM, Layton T, Hunt M. Asthma in United States Olympic athletes who participated in the 1996 Summer Games. J Allergy Clin Immunol. 1998; 102:722–726.
   PubMed Web of Science ®Google Scholar
• Global Initiative for Asthma. GINA report, global strategy for asthma management and prevention. 2006. Available at: http://www.ginasthma.org/.2011. Accessed January 8, 2012.
   Google Scholar
• Herxheimer H. Hyperventilation asthma. Lancet 1946; 1:83–87.
   PubMed Web of Science ®Google Scholar
• Strauss RH, McFadden, Jr., ER, Ingram, Jr., RH, Jaeger JJ. Enhancement of exercise-induced asthma by cold air. N Engl J Med. 1977; 297:743–747.
   PubMed Web of Science ®Google Scholar
• Stack MA, Hakemi A. Diagnosis and treatment of exercise-induced bronchospasm: a review. JAAPA 2011; 24:26–30.
   PubMedGoogle Scholar
• Parsons JP, Mastronarde JG. Exercise-induced bronchoconstriction in athletes. Chest 2005; 128:3966–3974.
   PubMed Web of Science ®Google Scholar
• Langdeau JB, Turcotte H, Bowie DM, Jobin J, Desgagne P, Boulet LP. Airway hyperresponsiveness in elite athletes. Am J Respir Crit Care Med. 2000; 161:1479–1484.
   PubMed Web of Science ®Google Scholar
• Helenius IJ, Tikkanen HO, Haahtela T. Association between type of training and risk of asthma in elite athletes. Thorax 1997; 52:157–160.
   PubMed Web of Science ®Google Scholar
• 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; 101:646–652.
   PubMed Web of Science ®Google Scholar
• Nystad W, Harris J, Borgen JS. Asthma and wheezing among Norwegian elite athletes. Med Sci Sports Exerc. 2000; 32:266–270.
   PubMed Web of Science ®Google Scholar
• Nowak D, Ulrik CS, Mutius vonE. Asthma and atopy: has peak prevalence been reached? Eur Respir J. 2004; 23:359–360.
   Google Scholar
• Rundell KW, Jenkinson DM. Exercise-induced bronchospasm in the elite athlete. Sports Med. 2002; 32:583–600.
   PubMed Web of Science ®Google Scholar
• Wilber RL, Rundell KW, Szmedra L, Jenkinson DM, Im J, Drakes D. Incidence of exercise-induced bronchospasm in Olympic winter sport athletes. Med Sci Sports Exerc. 2000; 32:732–737.
   PubMed Web of Science ®Google Scholar
• Weiler JM, Ryan, III, EJ. Asthma in United States Olympic athletes who participated in the 1998 Olympic winter games. J Allergy Clin Immunol. 2000; 106:267–271.
   PubMed Web of Science ®Google Scholar
• Anderson SD, Connolly NM, Godfrey S. Comparison of bronchoconstriction induced by cycling and running. Thorax 1971; 26:396–401.
   PubMed Web of Science ®Google Scholar
• 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; 5:152–159.
   PubMedGoogle Scholar
• Gotshall RW. Exercise-induced bronchoconstriction. Drugs 2002; 62:1725–1739.
   PubMed Web of Science ®Google Scholar
• Sue-Chu M, Henriksen AH, Bjermer L. Non-invasive evaluation of lower airway inflammation in hyper-responsive elite cross-country skiers and asthmatics. Respir Med. 1999; 93:719–725.
   PubMed Web of Science ®Google Scholar
• Larsson K, Ohlsen P, Larsson L, Malmberg P, Rydstrøm PO, Ulriksen H. High prevalence of asthma in cross country skiers. BMJ 1993; 307:1326–1329.
   PubMed Web of Science ®Google Scholar
• Weiler JM, Metzger WJ, Donnelly AL, Crowley ET, Sharath MD. Prevalence of bronchial hyperresponsiveness in highly trained athletes. Chest 1986; 90:23–28.
   PubMed Web of Science ®Google Scholar
• Mannix ET, Manfredi F, Farber MO. A comparison of two challenge tests for identifying exercise-induced bronchospasm in figure skaters. Chest 1999; 115:649–653.
   PubMed Web of Science ®Google Scholar
• Knopfli BH, Luke-Zeitoun M, von Duvillard SP, Burki A, Bachlecher C, Keller H. High incidence of exercise-induced bronchoconstriction in triathletes of the Swiss national team. Br J Sports Med. 2007; 41:486–491.
   PubMed Web of Science ®Google Scholar
• Lund TK, Pedersen L, Anderson SD, Sverrild A, Backer V. Are asthma-like symptoms in elite athletes associated with classical features of asthma? Br J Sports Med. 2009; 43:1131–1135.
   PubMed Web of Science ®Google Scholar
• Pohjantahti H, Laitinen J, Parkkari J. Exercise-induced bronchospasm among healthy elite cross country skiers and non-athletic students. Scand J Med Sci Sports. 2005; 15:324–328.
   PubMed Web of Science ®Google Scholar
• Hammerman SI, Becker JM, Rogers J, Quedenfeld TC, D'Alonzo GE, jr. Asthma screening of high school athletes: identifying the undiagnosed and poorly controlled. Ann Allergy Asthma Immunol. 2002; 88:380–384.
   PubMed Web of Science ®Google Scholar
• Rupp NT, Guill MF, Brudno DS. Unrecognized exercise-induced bronchospasm in adolescent athletes. Am J Dis Child. 1992; 146:941–944.
   PubMedGoogle Scholar
• Rupp NT, Brudno DS, Guill MF. The value of screening for risk of exercise-induced asthma in high school athletes. Ann Allergy. 1993; 70:339–342.
   PubMedGoogle Scholar
• Lund T, Pedersen L, Larsson B, Backer V. Prevalence of asthma-like symptoms, asthma and its treatment in elite athletes. Scand J Med Sci Sports. 2009; 19:174–178.
   PubMed Web of Science ®Google Scholar
• Helenius I, Rytila P, Sarna S, Lumme A, Helenius M, Remes V, Haahtela T. Effect of continuing or finishing high-level sports on airway inflammation, bronchial hyperresponsiveness, and asthma: a 5-year prospective follow-up study of 42 highly trained swimmers. J Allergy Clin Immunol. 2002; 109:962–968.
   PubMed Web of Science ®Google Scholar
• Dickinson JW, Whyte GP, McConnell AK, Harriess MG. Impact of changes in the IOC-MC asthma criteria: a British perspective. Thorax 2005; 60:629–632.
   PubMed Web of Science ®Google Scholar
• Voy RO. The U.S. Olympic Committee experience with exercise-induced bronchospasm, 1984. Med Sci Sports Exerc. 1986; 18:328–330.
   PubMed Web of Science ®Google Scholar
• Evans TM, Rundell KW, Beck KC, Levine AM, Baumann JM. Cold air inhalation does not affect the severity of EIB after exercise or eucapnic voluntary hyperventilation. Med Sci Sports Exerc. 2005; 37:544–549.
   PubMed Web of Science ®Google Scholar
• Helenius I, Haahtela T. Allergy and asthma in elite summer sport athletes. J Allergy Clin Immunol. 2000; 106:444–452.
   PubMed Web of Science ®Google Scholar
• Anderson SD. Is there a unifying hypothesis for exercise-induced asthma? J Allergy Clin Immunol 1984; 73:660–665.
   PubMed Web of Science ®Google Scholar
• Eggleston PA, Kagey-Sobotka A, Schleimer RP, Lichtenstein LM. Interaction between hyperosmolar and IgE-mediated histamine release from basophils and mast cells. Am Rev Respir Dis. 1984; 130:86–91.
   PubMed Web of Science ®Google Scholar
• Deal, Jr., EC, Wasserman SI, Soter NA, Ingram RH jr, McFadden ER jr. Evaluation of role played by mediators of immediate hypersensitivity in exercise-induced asthma. J Clin Invest. 1980; 65:659–665.
   PubMed Web of Science ®Google Scholar
• Anderson SD, Holzer K. Exercise-induced asthma: is it the right diagnosis in elite athletes? J Allergy Clin Immunol. 2000; 106:419–428.
   PubMed Web of Science ®Google Scholar
• Anderson SD, Daviskas E, Smith CM. Exercise-induced asthma: a difference in opinion regarding the stimulus. Allergy Proc. 1989; 10:215–226.
   PubMedGoogle Scholar
• 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; 158:1120–1126.
   PubMed Web of Science ®Google Scholar
• McFadden, Jr., ER. Exercise-induced asthma. Assessment of current etiologic concepts. Chest. 1987; 91:151S–157S.
   Web of Science ®Google Scholar
• McFadden, Jr., ER, Lenner KA, Strohl KP. Postexertional airway rewarming and thermally induced asthma. New insights into pathophysiology and possible pathogenesis. J Clin Invest. 1986; 78:18–25.
   PubMed Web of Science ®Google Scholar
• McFadden, Jr., ER. Hypothesis: exercise-induced asthma as a vascular phenomenon. Lancet. 1990; 335:880–883.
   PubMed Web of Science ®Google Scholar
• Makker HK, Holgate ST. Mechanisms of exercise-induced asthma. Eur J Clin Invest. 1994; 24:571–585.
   PubMed Web of Science ®Google Scholar
• Anderson SD, Daviskas E. The mechanism of exercise-induced asthma is. J Allergy Clin Immunol. 2000; 106:453–459.
   PubMed Web of Science ®Google Scholar
• Anderson SD, Kippelen P. Airway injury as a mechanism for exercise-induced bronchoconstriction in elite athletes. J Allergy Clin Immunol. 2008; 122:225–235.
   PubMed Web of Science ®Google Scholar
• Hallstrand TS, Moody MW, Wurfel MM, Schwartz LB, Hendersson WR, Aitken ML. Inflammatory basis of exercise-induced bronchoconstriction. Am J Respir Crit Care Med. 2005; 172:679–686.
   PubMed Web of Science ®Google Scholar
• O’Sullivan S, Roquet A, Dahlen B, Dahlen S, Kumlin M. Evidence for mast cell activation during exercise-induced bronchoconstriction. Eur Respir J. 1998; 12:345–350.
   PubMed Web of Science ®Google Scholar
• Reiss TF, Hill JB, Harman E, Zhang J, Tanaka WK, Bronsky E, Gurreiro D, Hendeles L. Increased urinary excretion of LTE4 after exercise and attenuation of exercise-induced bronchospasm by montelukast, a cysteinyl leukotriene receptor antagonist. Thorax 1997; 52:1030–1035.
   PubMed Web of Science ®Google Scholar
• Randolph C. An update on exercise-induced bronchoconstriction with and without asthma. Curr Allergy Asthma Rep. 2009; 9:433–438.
   PubMed Web of Science ®Google Scholar
• Nisar M, Spence DP, West D, Haycick J, Jones Y, Walshaw MJ, Earis JE, Claverley PM, Pearsson MG. A mask to modify inspired air temperature and humidity and its effect on exercise induced asthma. Thorax 1992; 47:446–450.
   PubMed Web of Science ®Google Scholar
• Carlsen KH, Anderson SD, Bjermer L, Bonini S, Brisasco V, Canonica W, Cummiskey J, Delgado L. Treatment of exercise-induced asthma, respiratory and allergic disorders in sports and the relationship to doping: part II of the report from the Joint Task Force of European Respiratory Society (ERS) and European Academy of Allergy and Clinical Immunology (EAACI) in cooperation with GA(2)LEN. Allergy 2008; 63:492–505.
   PubMed Web of Science ®Google Scholar
• Suissa S, Ernst P, Benayoun S, Baltzar M, Cai B. Low-dose inhaled corticosteroids and the prevention of death from asthma. N Engl J Med. 2000; 343:332–336.
   PubMed Web of Science ®Google Scholar
• Grzelewski T, Stelmach I. Exercise-induced bronchoconstriction in asthmatic children: a comparative systematic review of the available treatment options. Drugs 2009; 69:1533–1553.
   PubMed Web of Science ®Google Scholar
• Subbarao P, Duong M, Adelroth E, Otis J, Obminski G, Inman M, Pedersen S, O'Byrne PM. Effect of ciclesonide dose and duration of therapy on exercise-induced bronchoconstriction in patients with asthma. J Allergy Clin Immunol. 2006; 117:1008–1013.
   PubMed Web of Science ®Google Scholar
• Koh MS, Tee A, Lasserson TJ, Irving LB. Inhaled corticosteroids compared to placebo for prevention of exercise induced bronchoconstriction. Cochrane Database Syst Rev. 2007; CD002739.
   Google Scholar
• Sue-Chu M, Karjalainen EM, Laitinen A, Larsson L, Laitinen LA, Bjermer L. Placebo-controlled study of inhaled budesonide on indices of airway inflammation in bronchoalveolar lavage fluid and bronchial biopsies in cross-country skiers. Respiration 2000; 67:417–425.
   PubMed Web of Science ®Google Scholar
• Boot AM, de Jongste JC, Verberne AA, Pols HA, de Muinck Keizer-Schrane SM. Bone mineral density and bone metabolism of prepubertal children with asthma after long-term treatment with inhaled corticosteroids. Pediatr Pulmonol. 1997; 24:379–384.
   PubMed Web of Science ®Google Scholar
• Lipworth BJ. Systemic adverse effects of inhaled corticosteroid therapy: a systematic review and meta-analysis. Arch Intern Med. 1999; 159:941–955.
   PubMed Web of Science ®Google Scholar
• World Anti-Doping Agency. Available at: www.wada-ama.org. 2011. Accessed February 9, 2011.
   Google Scholar
• Anderson SD, Lambert S, Brannan JD, Wood RJ, Koskela M, Morton AR, Fitch KD. Laboratory protocol for exercise asthma to evaluate salbutamol given by two devices. Med Sci Sports Exerc. 2001; 33:893–900.
   PubMed Web of Science ®Google Scholar
• Ramage L, Lipworth BJ, Ingram CG, Cree IA, Dhillon DP. Reduced protection against exercise induced bronchoconstriction after chronic dosing with salmeterol. Respir Med. 1994; 88:363–368.
   PubMed Web of Science ®Google Scholar
• Simons FE, Gerstner TV, Cheang MS. Tolerance to the bronchoprotective effect of salmeterol in adolescents with exercise-induced asthma using concurrent inhaled glucocorticoid treatment. Pediatrics 1997; 99:655–659.
   PubMed Web of Science ®Google Scholar
• Weiler JM, Malloy C. Asthma and athletes: therapy to compete. Clin Rev Allergy Immunol. 2005; 29:139–149.
   PubMedGoogle Scholar
• Haney S, Hancox RJ. Recovery from bronchoconstriction and bronchodilator tolerance. Clin Rev Allergy Immunol. 2006; 31:181–196.
   PubMed Web of Science ®Google Scholar
• Hancox RJ, Subbarao P, Kamada D, Watson RM, Hargreave FE, Inman MD. Beta2-agonist tolerance and exercise-induced bronchospasm. Am J Respir Crit Care Med. 2002; 165:1068–1070.
   PubMed Web of Science ®Google Scholar
• Kollef M. SMART approaches for reducing nosocomial infections in the ICU. Chest 2008; 134:447–456.
   PubMed Web of Science ®Google Scholar
• Reynolds NA, Lyseng-Williamson KA, Wiseman LR. Inhaled salmeterol/fluticasone propionate: a review of its use in asthma. Drugs 2005; 65:1715–1734.
   Google Scholar
• Pauwels RA, Lofdahl CG, Postma DS, Tattersfield AE, O’Byrne PM, Barnes PJ, Ullman A. Effect of inhaled formoterol and budesonide on exacerbations of asthma. Formoterol and Corticosteroids Establishing Therapy (FACET) International Study Group. N Engl J Med. 1997; 337:1405–1411.
   PubMed Web of Science ®Google Scholar
• Hancox RJ, Taylor DR. Long-acting beta-agonist treatment in patients with persistent asthma already receiving inhaled corticosteroids. BioDrugs 2001; 15:11–24.
   PubMed Web of Science ®Google Scholar
• Elers J, Strandbygaard U, Pedersen L, Backer V. Daily use of salmeterol causes tolerance to bronchodilation with terbutaline in asthmatic subjects. Open Respir Med J. 2010; 4:48–50.
   PubMedGoogle Scholar
• Black JL, Oliver BG, Roth M. Molecular mechanisms of combination therapy with inhaled corticosteroids and long-acting beta-agonists. Chest 2009; 136:1095–1100.
   PubMed Web of Science ®Google Scholar
• Rundell KW, Spiering BA, Baumann JM, Evans TM. Effects of montelukast on airway narrowing from eucapnic voluntary hyperventilation and cold air exercise. Br J Sports Med. 2005; 39:232–236.
   PubMed Web of Science ®Google Scholar
• Helenius I, Lumme A, Ounap J, Obase Y, Rytila P, Sarna S, Alaranta A, Remes V, Haahtela T. No effect of montelukast on asthma-like symptoms in elite ice hockey players. Allergy 2004; 59:39–44.
   PubMed Web of Science ®Google Scholar
• McKenzie DC, McLuckie SL, Stirling DR. The protective effects of continuous and interval exercise in athletes with exercise-induced asthma. Med Sci Sports Exerc. 1994; 26:951–956.
   PubMed Web of Science ®Google Scholar
• Reiff DB, Choudry NB, Pride NB, Ind PW. The effect of prolonged submaximal warm-up exercise on exercise-induced asthma. Am Rev Respir Dis. 1989; 139:479–484.
   PubMed Web of Science ®Google Scholar
• Mickleborough TD, Lindley MR, Turner LA. Comparative effects of a high-intensity interval warm-up and salbutamol on the bronchoconstrictor response to exercise in asthmatic athletes. Int J Sports Med. 2007; 28:456–462.
   PubMed Web of Science ®Google Scholar
• Gilbert IA, Lenner KA, McFadden, Jr., ER. Sympathoadrenal response to repetitive exercise in normal and asthmatic subjects. J Appl Physiol. 1988; 64:2667–2674.
   PubMed Web of Science ®Google Scholar
• Belcher NG, Murdoch R, Dalton N, Clark TJ, Rees PJ, Lee TH. Circulating concentrations of histamine, neutrophil chemotactic activity, and catecholamines during the refractory period in exercise-induced asthma. J Allergy Clin Immunol. 1988; 81:100–110.
   PubMed Web of Science ®Google Scholar
• Manning PJ, Watson RM, O’Byrne PM. Exercise-induced refractoriness in asthmatic subjects involves leukotriene and prostaglandin interdependent mechanisms. Am Rev Respir Dis. 1993; 148:950–954.
   PubMedGoogle Scholar
• Rundell KW, Spiering BA, Judelson DA, Wilson MH. Bronchoconstriction during cross-country skiing: is there really a refractory period? Med Sci Sports Exerc. 2003; 35:18–26.
   PubMed Web of Science ®Google Scholar
• Miric M, Haxhiu MA. Effect of vitamin C on exercise-induced bronchoconstriction. Plucne Bolesti. 1991; 43:94–97.
   PubMedGoogle Scholar
• Mickleborough T, Gotshall R. Dietary components with demonstrated effectiveness in decreasing the severity of exercise-induced asthma. Sports Med. 2003; 33:671–681.
   PubMed Web of Science ®Google Scholar
• Christofidou-Solomidou M, Muzykantov VR. Antioxidant strategies in respiratory medicine. Treat Respir Med. 2006; 5:47–78.
   PubMedGoogle Scholar
• Cohen HA, Neuman I, Nahum H. Blocking effect of vitamin C in exercise-induced asthma. Arch Pediatr Adolesc Med. 1997; 151:367–370.
   PubMedGoogle Scholar
• Neuman I, Nahum H, Ben-Amotz A. Reduction of exercise-induced asthma oxidative stress by lycopene, a natural antioxidant. Allergy 2000; 55:1184–1189.
   PubMed Web of Science ®Google Scholar
• Schachter EN, Schlesinger A. The attenuation of exercise-induced bronchospasm by ascorbic acid. Ann Allergy. 1982; 49:146–151.
   PubMedGoogle Scholar
• Tecklenburg SL, Mickleborough TD, Fly AD, Bai Y, Stager JM. Ascorbic acid supplementation attenuates exercise-induced bronchoconstriction in patients with asthma. Respir Med. 2007; 101:1770–1778.
   PubMed Web of Science ®Google Scholar
• Mickleborough TD, Lindley MR, Ionescu AA, Fly AD. Protective effect of fish oil supplementation on exercise-induced bronchoconstriction in asthma. Chest 2006; 129:39–49.
   PubMed Web of Science ®Google Scholar
• Mickleborough TD, Murray RL, Ionescu AA, Lindley MR. Fish oil supplementation reduces severity of exercise-induced bronchoconstriction in elite athletes. Am J Respir Crit Care Med. 2003; 168:1181–1189.
   PubMed Web of Science ®Google Scholar
• VanHaitsma TA, Mickleborough T, Stager JM, Koceja DM, Lindley MR, Chapman R. Comparative effects of caffeine and albuterol on the bronchoconstrictor response to exercise in asthmatic athletes. Int J Sports Med. 2010; 31:231–236.
   PubMed Web of Science ®Google Scholar
• Chen WY, Horton DJ. Heat and water loss from the airways and exercise-induced asthma. Respiration 1977; 34:305–313.
   PubMed Web of Science ®Google Scholar
• Chen WY, Weiser PC, Chai H. Airway cooling. Stimulus for exercise-induced asthma. Scand J Respir Dis. 1979; 60:144–150.
   PubMedGoogle Scholar
• Millqvist E, Bengtsson U, Lowhagen O. Combining a beta2-agonist with a face mask to prevent exercise-induced bronchoconstriction. Allergy 2000; 55:672–675.
   PubMed Web of Science ®Google Scholar