Asthma and the elite athlete: Summary of the International Olympic Committee's Consensus Conference, Lausanne, Switzerland, January 22-24, 2008
2008; Elsevier BV; Volume: 122; Issue: 2 Linguagem: Inglês
10.1016/j.jaci.2008.07.003
ISSN1097-6825
AutoresKenneth D. Fitch, Malcolm Sue‐Chu, Sandra D. Anderson, Louis‐Philippe Boulet, Robert J. Hancox, Donald C. McKenzie, Vibeke Backer, Kenneth W. Rundell, Juan Manuel Alonso, Pascale Kippelen, Joseph Cummiskey, Alain Garnier, Arne Ljungqvist,
Tópico(s)Pharmacological Effects and Assays
ResumoRespiratory symptoms cannot be relied on to make a diagnosis of asthma and/or airways hyperresponsiveness (AHR) in elite athletes. For this reason, the diagnosis should be confirmed with bronchial provocation tests. Asthma management in elite athletes should follow established treatment guidelines (eg, Global Initiative for Asthma) and should include education, an individually tailored treatment plan, minimization of aggravating environmental factors, and appropriate drug therapy that must meet the requirements of the World Anti-Doping Agency. Asthma control can usually be achieved with inhaled corticosteroids and inhaled β2-agonists to minimize exercise-induced bronchoconstriction and to treat intermittent symptoms. The rapid development of tachyphylaxis to β2-agonists after regular daily use poses a dilemma for athletes. Long-term intense endurance training, particularly in unfavorable environmental conditions, appears to be associated with an increased risk of developing asthma and AHR in elite athletes. Globally, the prevalence of asthma, exercise-induced bronchoconstriction, and AHR in Olympic athletes reflects the known prevalence of asthma symptoms in each country. The policy of requiring Olympic athletes to demonstrate the presence of asthma, exercise-induced bronchoconstriction, or AHR to be approved to inhale β2-agonists will continue. Respiratory symptoms cannot be relied on to make a diagnosis of asthma and/or airways hyperresponsiveness (AHR) in elite athletes. For this reason, the diagnosis should be confirmed with bronchial provocation tests. Asthma management in elite athletes should follow established treatment guidelines (eg, Global Initiative for Asthma) and should include education, an individually tailored treatment plan, minimization of aggravating environmental factors, and appropriate drug therapy that must meet the requirements of the World Anti-Doping Agency. Asthma control can usually be achieved with inhaled corticosteroids and inhaled β2-agonists to minimize exercise-induced bronchoconstriction and to treat intermittent symptoms. The rapid development of tachyphylaxis to β2-agonists after regular daily use poses a dilemma for athletes. Long-term intense endurance training, particularly in unfavorable environmental conditions, appears to be associated with an increased risk of developing asthma and AHR in elite athletes. Globally, the prevalence of asthma, exercise-induced bronchoconstriction, and AHR in Olympic athletes reflects the known prevalence of asthma symptoms in each country. The policy of requiring Olympic athletes to demonstrate the presence of asthma, exercise-induced bronchoconstriction, or AHR to be approved to inhale β2-agonists will continue. In response to a marked increase in the notification by athletes of use of inhaled β2-agonists from 3.7% in Atlanta in 1996 to 5.6% at the 1998 Winter Games in Nagano, and to 5.7% in Sydney in 2000, the International Olympic Committee's (IOC's) Medical Commission conducted a symposium on asthma in 2001. Concerned that athletes without asthma may have been using inhaled β2-agonists, the symposium recommended that to be granted permission to use inhaled β2-agonists at future Games, athletes should be required to demonstrate current asthma, exercise-induced asthma, exercise-induced bronchoconstriction (EIB), or airway hyperresponsiveness (AHR). For further detail, see “Why inhaled β2-agonists are prohibited and why the IOC has introduced its policy on inhaled β2-agonists” in the Online Repository at www.jacionline.org. The IOC agreed with the recommendation, which was made for health and not doping reasons. Subsequent publications have reviewed the consequences of this decision at the Olympics in 20021Anderson S.D. Fitch K. Perry C.P. Sue-Chu M. Crapo R. McKenzie D. et al.Responses to bronchial challenge submitted for approval to use inhaled beta2 agonists prior to an event at the 2002 Winter Olympics.J Allergy Clin Immunol. 2003; 111: 44-49Abstract Full Text Full Text PDF Scopus (100) Google Scholar and in 20042Anderson S.D. Sue-Chu M. Perry C.P. Gratziou C. Kippelen P. McKenzie D.C. et al.Bronchial challenges in athletes applying to inhale a beta2-agonist at the 2004 Summer Olympics.J Allergy Clin Immunol. 2006; 117: 767-773Abstract Full Text Full Text PDF PubMed Scopus (75) Google Scholar and provided an overview of β2-agonists at the Olympic Games.3Fitch K.D. b2-Agonists at the Olympic Games.Clin Rev Allergy Immunol. 2006; 31: 259-268Crossref PubMed Scopus (51) Google Scholar In 2003, the International Association of Athletics Federations (IAAF) introduced the same requirements and criteria as the IOC. At a conference in January 2008, the IOC re-examined this topic, a decision in part provoked by the World Anti-Doping Agency (WADA) seeking clarification for the differences in policy between the IOC and WADA with respect to β2-agonists. The conference examined a number of issues including the diagnosis and optimal treatment of asthma, EIB and AHR in elite athletes, past experience of β2-agonists before and after the need to obtain approval, environmental and genetic aspects (see “Genetic aspects of asthma” in the Online Repository at www.jacionline.org), intense endurance training as a possible cause of asthma/AHR, the performance of athletes inhaling β2-agonists, and the future of β2-agonists at Olympic Games. This is a review of the conference proceedings and the consensus statement (see “IOC consensus statement on asthma in elite athletes” in the Online Repository at www.jacionline.org) prepared at the conclusion of the meeting. Asthma is a syndrome with many clinical phenotypes.4Standards for the diagnosis and care of patients with chronic obstructive pulmonary disease (COPD) and asthma. This official statement of the American Thoracic Society was adopted by the ATS Board of Directors, November 1986.Am Rev Respir Dis. 1987; 136: 225-244Crossref PubMed Scopus (2871) Google Scholar Exercise-induced asthma is the occurrence of a transient narrowing of the airways after exercise that is reversible by inhalation of a β2-agonist in an individual with asthma. When narrowing of the airways occurs only with exercise, this phenomenon is best described as EIB.5Anderson S.D. Daviskas E. The mechanism of exercise-induced asthma is….J Allergy Clin Immunol. 2000; 106: 453-459Abstract Full Text Full Text PDF PubMed Scopus (404) Google Scholar The term EIB is self-explanatory and is used throughout this article. Sports activities at an elite level are often associated with symptoms that may be suggestive of asthma. These include breathlessness, wheeze, cough, chest tightness, and phlegm in relation to exercise. Of these, breathlessness is the dominant symptom, reported in almost 50% of winter athletes. In contrast, wheezing and waking with breathlessness are less prevalent in athletes than in the general population.6Turcotte H. Langdeau J.B. Thibault G. Boulet L.P. Prevalence of respiratory symptoms in an athlete population.Respir Med. 2003; 97: 955-963Abstract Full Text Full Text PDF PubMed Scopus (46) Google Scholar Epidemiologic studies suggest that self-reported and physician-diagnosed asthma are twice as common in elite Norwegian7Nystad W. Harris J. Borgen J.S. Asthma and wheezing among Norwegian elite athletes.Med Sci Sports Exerc. 2000; 32: 266-270Crossref PubMed Scopus (69) Google Scholar and Finnish athletes8Alaranta A. Alaranta H. Palmu P. Alha P. Pietila K. Heliovaara M. et al.Asthma medication in Finnish Olympic athletes: no signs of inhaled beta2-agonist overuse.Med Sci Sports Exerc. 2004; 36: 919-924Crossref PubMed Scopus (43) Google Scholar than in randomly selected age-matched and sex-matched control populations. The higher prevalence of asthma reported in athletes may be a result of overdiagnosis, particularly because a diagnosis of asthma is often made on the basis of the history alone.9Parsons J.P. O'Brien J.M. Lucarelli M.R. Mastronarde J.G. Differences in the evaluation and management of exercise-induced bronchospasm between family physicians and pulmonologists.J Asthma. 2006; 43: 379-384Crossref PubMed Scopus (24) Google Scholar A clinical suspicion of asthma should ideally be confirmed by demonstrating either a 12% increase in FEV1 from the baseline or predicted value in response to a bronchodilator or AHR (see “Bronchial provocation tests”). In elite winter sports athletes, 2 or more symptoms suggestive of asthma had a sensitivity and specificity of 50% and 78%, respectively, for the presence of EIB assessed with a field-based exercise test.10Rundell K.W. Im J. Mayers L.B. Wilber R.L. Szmedra L. Schmitz H.R. Self-reported symptoms and exercise-induced asthma in the elite athlete.Med Sci Sports Exerc. 2001; 33: 208-213Crossref PubMed Scopus (264) Google Scholar Asthma was misdiagnosed in 21% and undiagnosed in 2.6% of athletes in the 2004 British Summer Olympic team.11Dickinson J.W. Whyte G.P. McConnell A.K. Harries M.G. Impact of changes in the IOC-MC asthma criteria: a British perspective.Thorax. 2005; 60: 629-632Crossref PubMed Scopus (71) Google Scholar In the absence of objective tests of airway function, other diagnoses such as upper airway dysfunction may be overlooked. Bronchial provocation tests (BPTs) are used to identify AHR and to aid the diagnosis of asthma in athletes. The 2 types of BPTs are indirect and direct. The indirect tests include exercise, eucapnic voluntary hyperpnea (EVH; also known as the isocapnic hyperventilation test) and hyperosmolar aerosols such as 4.5% saline and mannitol.12Joos G.F. O'Connor B. Anderson S.D. Chung F. Cockcroft D.W. Dahlén B. et al.ERS Task Force. Indirect airway challenges.Eur Respir J. 2003; 21: 1050-1068Crossref PubMed Scopus (304) Google Scholar These stimuli act indirectly to cause airway smooth muscle (ASM) contraction and airway narrowing by release of mediators (eg, prostaglandins, leukotrienes, and histamine) from inflammatory cells in the airways. The fall in FEV1 from the baseline value used to define abnormality is the mean plus 2 SDs of the fall documented in healthy subjects without asthma in response to the maximum dose of the test stimulus. For exercise and EVH, a fall in FEV1 of 10% is consistent with EIB.13Crapo R.O. Casaburi R. Coates A.L. Enright P.L. Hankinson J.L. Irvin C.G. et al.Guidelines for methacholine and exercise challenge testing - 1999.Am J Respir Crit Care Med. 2000; 161: 309-329Crossref PubMed Scopus (2160) Google Scholar, 14Anderson S.D. Argyros G.J. Magnussen H. Holzer K. Provocation by eucapnic voluntary hyperpnoea to identify exercise induced bronchoconstriction.Br J Sports Med. 2001; 35: 344-347Crossref PubMed Scopus (210) Google Scholar A fall in FEV1 of 15% in response to 4.5% saline or mannitol is consistent with a clinical diagnosis of asthma with or without EIB.15Brannan J.D. Anderson S.D. Perry C.P. Freed-Martens R. Lassig A.R. Charlton B. The safety and efficacy of inhaled dry powder mannitol as a bronchial provocation test for airway hyperresponsiveness: a phase 3 comparison study with hypertonic (4.5%) saline.Respir Res. 2005; 6: 144Crossref PubMed Scopus (168) Google Scholar A positive response to indirect stimuli is consistent with airway inflammation.16Koskela H. Hyvärinen L. Brannan J.D. Chan H.-K. Anderson S.D. Sensitivity and validity of three bronchial provocation tests to demonstrate the effect of inhaled corticosteroids in asthma.Chest. 2003; 124: 1341-1349Crossref PubMed Scopus (54) Google Scholar After 3 to 8 weeks of treatment with inhaled corticosteroids (ICSs), 50% of subjects can expect remission of their EIB.17Hofstra W.B. Neijens H.J. Duiverman E.J. Kouwenberg J.M. Mulder P.G. Kuethe M.C. et al.Dose-response over time to inhaled fluticasone propionate: treatment of exercise- and methacholine-induced bronchoconstriction in children with asthma.Pediatr Pulmonol. 2000; 29: 415-423Crossref PubMed Scopus (102) Google Scholar, 18Subbarao P. Duong M. Adelroth E. Otis J. Obminski G. 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A comparison of two challenge tests for identifying exercise-induced bronchospasm in figure skaters.Chest. 1999; 115: 649-653Crossref PubMed Scopus (94) Google Scholar Because it is the ventilation (rather than the heart rate) and the water content of the air inspired24Anderson S.D. Schoeffel R.E. Follet R. Perry C.P. Daviskas E. Kendall M. Sensitivity to heat and water loss at rest and during exercise in asthmatic patients.Eur J Respir Dis. 1982; 63: 459-471PubMed Google Scholar that are the most important factors for identifying EIB, alternative tests were sought to encompass these factors. The EVH test was developed as a surrogate for exercise to test for EIB.25Phillips Y.Y. Jaeger J.J. Laube B.L. Rosenthal R.R. Eucapnic voluntary hyperventilation of compressed gas mixture: a simple system for bronchial challenge by respiratory heat loss.Am Rev Respir Dis. 1985; 131: 31-35PubMed Google Scholar It requires the subject to ventilate between 22 to 30 times FEV1 (L; preferably 30 times) for 6 minutes while breathing dry air containing 5% carbon dioxide.14Anderson S.D. Argyros G.J. Magnussen H. Holzer K. Provocation by eucapnic voluntary hyperpnoea to identify exercise induced bronchoconstriction.Br J Sports Med. 2001; 35: 344-347Crossref PubMed Scopus (210) Google Scholar The test duration, temperature, and ventilation level can be varied to simulate the conditions of the sport. EVH has been compared with exercise and other stimuli and is now well established for assessing elite athletes.1Anderson S.D. Fitch K. Perry C.P. Sue-Chu M. Crapo R. McKenzie D. et al.Responses to bronchial challenge submitted for approval to use inhaled beta2 agonists prior to an event at the 2002 Winter Olympics.J Allergy Clin Immunol. 2003; 111: 44-49Abstract Full Text Full Text PDF Scopus (100) Google Scholar, 11Dickinson J.W. Whyte G.P. McConnell A.K. Harries M.G. Impact of changes in the IOC-MC asthma criteria: a British perspective.Thorax. 2005; 60: 629-632Crossref PubMed Scopus (71) Google Scholar, 14Anderson S.D. Argyros G.J. Magnussen H. Holzer K. Provocation by eucapnic voluntary hyperpnoea to identify exercise induced bronchoconstriction.Br J Sports Med. 2001; 35: 344-347Crossref PubMed Scopus (210) Google Scholar, 23Mannix E.T. Manfredi F. Farber M.O. A comparison of two challenge tests for identifying exercise-induced bronchospasm in figure skaters.Chest. 1999; 115: 649-653Crossref PubMed Scopus (94) Google Scholar, 26Rundell K.W. Anderson S.D. Spiering B.A. Judelson D.A. 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Hyperosmolarity as the stimulus to asthma induced by hyperventilation?.J Allergy Clin Immunol. 1986; 77: 729-736Abstract Full Text PDF PubMed Scopus (84) Google Scholar Hyperosmolar (4.5%) saline is inhaled during tidal breathing as a wet aerosol generated by a large-volume ultrasonic nebulizer. Alternatively, mannitol powder can be delivered from capsules by using a dry powder inhaler. The clinical efficacy and safety of mannitol to identify AHR have been established,15Brannan J.D. Anderson S.D. Perry C.P. Freed-Martens R. Lassig A.R. Charlton B. The safety and efficacy of inhaled dry powder mannitol as a bronchial provocation test for airway hyperresponsiveness: a phase 3 comparison study with hypertonic (4.5%) saline.Respir Res. 2005; 6: 144Crossref PubMed Scopus (168) Google Scholar and the test is registered for this indication in Australia, Europe, and Korea. The direct stimulus most often used to evaluate athletes is methacholine chloride. Methacholine stimulates acetylcholine receptors to cause smooth muscle contraction. The fall in FEV1 in response to a particular concentration or dose provides an index of sensitivity of the ASM to methacholine. Because healthy people can also respond to methacholine, it has been necessary to select an adequate dose or concentration to define hyperresponsiveness.30Eiser N.M. Kerrebijn K.F. Quanjer P.H. Guidelines for standardization of bronchial challenge with (nonspecific) bronchoconstricting agents. Working Group on Bronchial Hyperreactivity SEPCR.Bull Eur Physiopathol Respir. 1983; 19: 495-514PubMed Google Scholar There are a number of different techniques and devices used to deliver methacholine, making it difficult to be precise about dose/concentration equivalents, and concentration only is used in some guidelines.13Crapo R.O. Casaburi R. Coates A.L. Enright P.L. Hankinson J.L. Irvin C.G. et al.Guidelines for methacholine and exercise challenge testing - 1999.Am J Respir Crit Care Med. 2000; 161: 309-329Crossref PubMed Scopus (2160) Google Scholar A provoking concentration to cause a 20% fall in FEV1 (PC20) of ≤1 mg/mL has a very high specificity for identifying clinically recognized asthma in young adults.31Cockcroft D.W. Murdock K.Y. Berscheid B.A. Gore B.P. Sensitivity and specificity of histamine PC20 determination in a random selection of young college students.J Allergy Clin Immunol. 1992; 89: 23-30Abstract Full Text PDF PubMed Scopus (138) Google Scholar A PC20 of ≤4 mg/mL is equivalent to a cumulative provoking dose (PD20) of 400 μg or a noncumulative PD20 of 200 μg and identifies people with mild, moderate, and severe AHR.13Crapo R.O. Casaburi R. Coates A.L. Enright P.L. Hankinson J.L. Irvin C.G. et al.Guidelines for methacholine and exercise challenge testing - 1999.Am J Respir Crit Care Med. 2000; 161: 309-329Crossref PubMed Scopus (2160) Google Scholar, 32Yan K. Salome C. Woolcock A.J. Rapid method for measurement of bronchial responsiveness.Thorax. 1983; 38: 760-765Crossref PubMed Scopus (585) Google Scholar The criteria for identifying AHR in those taking ICS are higher (a PC20 of ≤16 mg/mL, or PD20 of 1600 μg and 800 μg for cumulative and noncumulative doses, respectively).13Crapo R.O. Casaburi R. Coates A.L. Enright P.L. Hankinson J.L. Irvin C.G. et al.Guidelines for methacholine and exercise challenge testing - 1999.Am J Respir Crit Care Med. 2000; 161: 309-329Crossref PubMed Scopus (2160) Google Scholar In elite summer athletes, the sensitivity of methacholine to identify EIB has been reported to be low and less than 40%.27Holzer K. Anderson S.D. Douglass J. Exercise in elite summer athletes: challenges for diagnosis.J Allergy Clin Immunol. 2002; 110: 374-380Abstract Full Text Full Text PDF PubMed Scopus (170) Google Scholar, 33Pedersen L. Winther S. Backer V. Anderson S.D. Larsen K.R. Airway responses to eucapnic hyperpnea, exercise and methacholine in elite swimmers.Med Sci Sports Exerc. 2008; (In press)Google Scholar, 34Bougault V. Turmel J. Boulet L.P. Respiratory symptoms and prevalence of airway hyperresponsiveness (AHR) in elite swimmers.Am J Respir Crit Care Med. 2008; 177: A998Google Scholar This low sensitivity to identify AHR is thought to relate to the greater potency of the mediators (prostaglandins and leukotrienes) released in response to the indirect stimuli compared with methacholine in healthy fit subjects with good lung function.35Barnes N.C. Piper P.J. Costello J.F. 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Exercise-induced bronchoconstriction: pathogenesis.Curr Allergy Asthma Rep. 2005; 5: 116-122Crossref PubMed Scopus (114) Google Scholar Tests using other pharmacologic agents such as carbachol, histamine, or AMP have not been accepted by the IOC's Medical Commission. For the 2004 Games in Athens, 3 countries had 50 or more applicants (Australia, 67; Great Britain, 54; United States, 53). Of these 174 applicants, 17% submitted results of a bronchodilator test, 59% an EVH or exercise challenge, 15% a hypertonic saline challenge, and 9% methacholine tests.39Anderson S.D. Brusasco V. Haahtela T. Popov T. Criteria for diagnosis of asthma, exercise-induced bronchoconstriction and airway hyperresponsiveness for athlete: lessons from the Olympic Games.Eur Respir Mon. 2005; 33: 48-66Crossref Google Scholar The goal of asthma treatment is to reduce or prevent respiratory symptoms and to optimize pulmonary function.40Global Strategy for Asthma Management and Prevention.Global Initiative for Asthma (GINA). 2006; (Available at:) (Accessed July 15, 2008)http://www.ginasthma.orgGoogle Scholar Management of asthma in athletes should be similar to management in nonathletes, with attention to patient education (which is often deficient in athletes),41Kuehn B.M. Education key to treating airway disease: focus on inhaler users, rescue workers, athletes.JAMA. 2007; 298: 2601-2608Crossref PubMed Scopus (4) Google Scholar reduction of relevant environmental exposures, treatment of associated comorbid conditions, individualized pharmacotherapy, prevention of exacerbations, and regular follow-up (Fig 1). Athletes should also be advised to avoid training when air quality is impaired and under extreme conditions of temperature and humidity. The use of a face mask attenuates EIB in athletes breathing cold air and has a synergistic effect when combined with β2-agonists.42Millqvist E. Bengtsson U. Lowhagen O. Combining a beta2-agonist with a face mask to prevent exercise-induced bronchoconstriction.Allergy. 2000; 55: 672-675Crossref PubMed Scopus (27) Google Scholar Although the high ventilation in these athletes makes these masks difficult to use during competition, use of these heat and moisture exchangers should be encouraged during training sessions. Measures to reduce chlorine derivatives in swimming pools, as well as ozone and particulate matter (PM) in indoor sports arenas, should be considered. Pharmacotherapy should aim to attenuate EIB. This is best achieved by the use of ICSs for an adequate time.18Subbarao P. Duong M. Adelroth E. Otis J. Obminski G. Inman M. et al.Effect of ciclesonide dose and duration of therapy on exercise-induced bronchoconstriction in patients with asthma.J Allergy Clin Immunol. 2006; 117: 1008-1013Abstract Full Text Full Text PDF PubMed Scopus (72) Google Scholar If EIB is still not controlled despite efficient inhaler technique and good compliance, the dose of ICS can be increased or treatment can be supplemented with another medication, such as a long-acting β2-agonist or a leukotriene antagonist, sodium cromoglycate, or nedocromil sodium.20Rundell K. Spiering B.A. Baumann J.M. Evans T.M. Effects of montelukast on airway narrowing from eucapnic voluntary hyperventilation and cold air exercise.Br J Sports Med. 2005; 39: 232-236Crossref PubMed Scopus (51) Google Scholar, 21Pearlman D.S. van Adelsberg J. Philip G. Tilles S.A. Busse W. 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Athletes with asthma will need a fast-acting bronchodilator. Inhaled β2-agonists are the most effective bronchodilators for the relief of asthma symptoms and for pretreatment of EIB.50Bateman E.D. Hurd S.S. Barnes P.J. Bousquet J. Drazen J.M. FitzGerald M. et al.Global strategy for asthma management and prevention: GINA executive summary.Eur Respir J. 2008; 31: 143-178Crossref PubMed Scopus (2285) Google Scholar In addition, long-acting β2-agonists are often combined with inhaled corticosteroids to improve asthma control.50Bateman E.D. Hurd S.S. Barnes P.J. Bousquet J. Drazen J.M. FitzGerald M. et al.Global strategy for asthma management and prevention: GINA executive summary.Eur Respir J. 2008; 31: 143-178Crossref PubMed Scopus (2285) Google Scholar Unfortunately, studies show that regular treatment with β2-agonists increases the sensitivity of the airways to bronchoconstrictive stimuli including exercise and allergens (see this article's Fig E1 in the Online Repository at www.jacionline.org). Athletes who have been using β2-agonists regularly or frequently are likely to experience worsening of EIB if they do not take them before exercise. In addition, both the bronchodilator and the bronchoprotective effects of β2-agonists diminish after a few days of regular use. Hence athletes using regular or frequent β2-agonists will have reduced protection against EI
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