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Exercise-Induced Bronchoconstriction in Athletes* FREE TO VIEW

Jonathan P. Parsons, MD; John G. Mastronarde, MD, FCCP
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*From the Division of Pulmonary and Critical Care Medicine, Department of Internal Medicine, The Ohio State University, Columbus, OH.

Correspondence to: Jonathan P. Parsons, MD, Division of Pulmonary and Critical Care Medicine, The Ohio State University, 201 HLRI, 473 W 12th Ave, Columbus, OH 43210; e-mail: Johnathan.Parsons@osumc.edu



Chest. 2005;128(6):3966-3974. doi:10.1378/chest.128.6.3966
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Exercise-induced bronchoconstriction (EIB) describes airway narrowing that occurs in association with exercise. EIB occurs in up to 90% of asthmatic patients and is estimated to occur in > 10% of the general population. Recent reviews have identified asthma as a risk factor for sudden death and have reported many deaths that have been attributed directly to EIB. We present a review of the literature related to EIB in athletes including sections discussing its pathogenesis, diagnosis, and treatment, and which athletes are most at risk for experiencing EIB.

Figures in this Article

Exercise-induced bronchoconstriction (EIB) describes acute, transient airway narrowing that occurs during and most often after exercise. EIB objectively is defined as a ≥ 10% decline in FEV1 after appropriate exercise provocation.1Exercise is the most common trigger of bronchospasm in those who are known to be asthmatic, and 50 to 90% of all individuals with asthma have airways that are hyperreactive to exercise.2However, EIB also occurs in up to 10% of subjects who are not known to be atopic or asthmatic.3

The public health consequences of unrecognized or inadequately treated EIB are significant. In reviewing > 30 years of Israeli military recruit data, Amital et al4found that asthma was the single greatest risk factor for unexplained death. Becker et al5 identified 61 deaths over a 7-year period that met the criteria of an asthma death occurring in close association with a sporting event or physical activity. Of these deaths, 81% occurred in subjects who were younger than 21 years of age and 57% occurred in subjects who were considered to be elite or competitive. Strikingly, almost 10% of deaths in this review occurred in subjects with no known history of asthma or EIB. Results from these reviews suggest that all individuals involved in organized sports or physical activity should be cognizant of the risk of EIB. Coaches, trainers, and team physicians who care for competitive athletes who have asthma or EIB should be specifically trained in the recognition and treatment of EIB.

The prevalence rates of bronchospasm related to exercise in athletes range from 11 to 50%2 (Table 1 ), and up to 90% of subjects with asthma will have EIB.,6Wilber at al7found that 18 to 26% of Olympic winter sport athletes and 50% of cross-country skiers were found to have EIB. Of the 50 elite summer athletes studied, with and without asthma, Holzer et al8found 50% to have EIB. Mannix et al9studied 124 elite figure skaters and tested them on an ice rink during their figure-skating routines. Thirty-five percent had a significant postexercise drop in their FEV1. The US Olympic Committee10 reported an 11.2% prevalence of EIB in all athletes who competed in the 1984 summer Olympics.

Despite numerous studies that have investigated the prevalence of EIB in athletes, most either included asthmatic patients in their data analysis or did not indicate what proportion were asthmatic prior to study enrollment, which makes it difficult to accurately estimate the prevalence of EIB in nonasthmatic athletes. Few studies have investigated the prevalence of EIB in cohorts of athletes without a known history of asthma or EIB. Rupp et al11evaluated 230 middle school and high school student athletes and, after excluding those with known EIB, found that 29% had a ≥ 15% reduction in their FEV1 after exercise challenge. Weiler et al12 found that 12% of college football players at the University of Iowa admitted to a history of asthma, 19% had respiratory symptoms postexercise, and 50% had evidence of bronchial hyperreactivity after bronchoprovocation. When members at an urban fitness center were studied, Mannix et al13 found that 41 of 212 subjects (19%), none of whom had previously received a diagnosis of asthma, had EIB. These studies suggested that EIB occurs frequently in subjects who are not known to be asthmatic and likely is underdiagnosed clinically.

The prevalence of EIB in athletes may be further underappreciated as patients with asthma and hyperreactive airways have been shown to be poor perceivers of symptoms of bronchospasm.1416 Athletes, specifically, often experience a lack of awareness of symptoms that are suggestive of EIB.1718 Athletes are generally fit and healthy, and the presence of a significant medical problem often is not considered. The athlete is often considered to be “out of shape,” and vague symptoms of chest discomfort, breathlessness, and fatigue may not be interpreted as a manifestation of EIB. Athletes themselves are often not aware that they may have a physical problem. Furthermore, if they do recognize they have a medical problem, they often do not want to admit to health personnel that a problem exists.19

The pathogenesis of EIB is likely multifactorial and is not completely understood. The predominant hypothesis for the etiology of EIB is that breathing relatively dry air causes the airways to narrow by osmotic and thermal consequences of evaporative water loss from the airway surface.20These stimuli have been demonstrated to cause cough21and mucus production22independently in patients without predisposing respiratory conditions such as asthma. The hyperosmolar environment created by evaporative water loss may result in the release of mediators such as histamine, which is a potent bronchoconstrictor, from mast cell degranulation.23

During exercise, large volumes of air that are often colder than body temperature are exchanged. This large volume of air often overwhelms the ability of the upper airway to warm the air effectively, and, consequently, cool air reaches the distal airways. It has been suggested that cold air in the distal airways results in airway narrowing due to reactive hyperemia of the bronchial vasculature, and the subsequent increased hydrostatic pressures in the capillary bed lead to airway edema.24Kanazawa et al25 found that increased airway vascular permeability correlates with the severity of EIB in asthmatic patients. These data suggest that vascular responses in the distal capillaries are likely to be involved in the development of EIB.

Inflammation also plays an important role in the pathogenesis of EIB in asthmatic subjects. Asthma results from a chronic inflammatory cascade that ultimately results in airway inflammation, mucus production, smooth muscle hypertrophy, and bronchospasm.26A significant correlation has been reported between the severity of EIB and the degree of peripheral blood eosinophilia27and eosinophilic inflammation in induced sputum28 in asthmatic patients.

Although inflammation is a critical component of asthma and EIB that occurs in asthmatic patients, the role or significance of inflammation in the pathogenesis of EIB in subjects without asthma is unclear. The term exercise-induced asthma is often used interchangeably with EIB; however, EIB that occurs in athletes without a history of asthma who have normal lung function may be a distinct phenomenon from bronchospasm occurring as a manifestation of asthma. While the relationship between inflammation and airway hyperresponsiveness in nonasthmatic EIB patients is not well-understood, some evidence suggests that inflammation is increased in the airways of subjects without asthma after exercise or hyperventilation challenge. Karjalainen et al29measured mucosal inflammatory cell infiltration in the subepithelial basement membrane in endobronchial biopsy specimens of the proximal airways from 40 elite skiers without asthma. Biopsy specimens from the elite skiers were compared to biopsy specimens of 12 asthmatic subjects. The authors found that skiers had a greater degree of neutrophil infiltration, which is not typical in either atopic or nonatopic asthma. Furthermore, skiers had a lesser degree of infiltration with eosinophils, mast cells, and macrophages. These results suggest that the inflammatory process in these athletes may be different from that in asthmatic individuals. Larsson et al30found that a short exposure to cold air while running induced an increase in the number of granulocytes and macrophages in the BAL fluid of healthy subjects. Repetitive hyperpnea itself has been shown to recruit eosinophils to the airways and to promote the release of inflammatory cytokines.31 Although inflammatory cells have been documented in the airways of nonasthmatic subjects, whether they play a direct role in the development of airway hyperresponsiveness in nonasthmatic athletes that experience EIB is not known.

Exhaled nitric oxide (NO) is emerging as a new technique that may help to identify subjects with airway inflammation. EIB is currently thought to occur in part due to vasomotor changes related to relatively cool air in the distal airways. Because NO has profound effects on airway and vasomotor tone, it may be intimately involved in mediating the thermal consequences of exercise. Kotaru et al32 demonstrated that during hyperventilation asthmatic subjects generated approximately 55% more NO per minute than did healthy control subjects, even though their level of ventilation was approximately 66% lower. In contrast to healthy subjects, NO production in the asthmatic patients continued into the recovery period after the challenge stopped, and the fraction of exhaled NO rose temporally as the airflow limitation developed. These results suggest that NO plays a significant role in the development of airway obstruction that follows hyperventilation, and the quantification of exhaled NO may help to identify athletes who are at risk for experiencing EIB.

Although athletes who compete in high-ventilation or endurance sports (Table 2 ) are more likely to experiences symptoms of EIB than those who participate in low-ventilation sports,33 EIB can occur in any setting.13 It is especially prevalent in endurance events such as cross-country skiing, swimming, and long-distance running33 in which ventilation is increased for long periods of time during training and competition, allowing for relatively more evaporative water loss and subsequent airway narrowing. There is also increased prevalence of EIB in winter sports athletes,7 which is thought to be due in part to the increased cooling of airways and the relative increase in reactive hyperemia in the pulmonary vasculature. It is important for athletes, coaches, and trainers supervising athletes in these “higher risk” sports to be aware of the increased incidence of EIB in these populations of athletes.

Athletes who participate in environments in which there may be environmental pollutants are at increased risk for the development of EIB. Chlorine compounds in swimming pools34and chemicals related to ice-resurfacing machinery in ice rinks35 may put certain populations of athletes at additional risk. Particulate matter and gases such as carbon monoxide and nitrogen dioxide, which are abundant in indoor ice arenas, and chlorine from swimming pools may act as allergic “triggers” and may exacerbate bronchospasm in athletes who are predisposed to EIB. Helenius and Haahtela34 showed a 96-fold greater risk of asthma in atopic swimmers when compared to nonatopic control subjects when atopy and swimming were included in multivariate statistical analysis. Leuppi et al36 found a 35% incidence of airway hyperresponsiveness in a group of ice-hockey players. In addition, figure skaters have been shown to have a high incidence of EIB.7,9

The clinical manifestations of EIB can range from mild impairment of performance to, less commonly, severe bronchospasm and respiratory failure. Common symptoms include coughing, wheezing, chest tightness, and dyspnea. More subtle evidence of EIB includes fatigue, symptoms that occur in specific environments (ie, ice rinks or swimming pools), poor performance for conditioning level, and avoidance of activity.

Generally, an exercise duration of 5 to 8 min at a workload representing at least 80% of the maximal predicted oxygen consumption is required to generate bronchospasm in most athletes.37Typically, athletes experience transient bronchodilation during exercise and experience symptoms of EIB shortly after exercise. Usually, symptoms peak 5 to 10 min after exercise ceases and can remain significant for 30 min if no bronchodilator therapy is provided.38 Even in the absence of intervention with bronchodilator therapy, many athletes will spontaneously recover to baseline airflow within 60 min.37 Athletes who experience symptoms for extended periods often perform at suboptimal levels for significant portions of their competitive or recreational activities.

The presence of EIB has been shown to be difficult to diagnose clinically as symptoms are often nonspecific.33 The lack of standard diagnostic methodology in the past is partly responsible for the large variability in the reported prevalence of EIB across different sports.2Figure 1 demonstrates our clinical approach to the diagnosis of EIB. A complete history should be taken and a complete physical examination should be performed on each athlete who has respiratory complaints associated with exercise. Other medical problems that can mimic EIB and that need to be considered in the initial evaluation of exertional dyspnea include vocal cord dysfunction, cardiac arrhythmias, and pulmonary or cardiac shunts. A comprehensive history and physical examination are recommended to help rule out these disorders; however, the examination findings are often normal in athletes with EIB. A history of specific symptoms in particular environments or during specific activities should be elicited. A thorough family and occupational history should also be obtained, as a family history of asthma increases the risk of a family member developing asthma.39

Despite the value of a comprehensive history of the athlete with exertional dyspnea, the diagnosis of EIB based on self-reported symptoms alone has been shown to be inaccurate. Rundell et al17 demonstrated that only 61% of EIB-positive athletes reported symptoms of EIB, while 45% of athletes with normal pulmonary function reported symptoms. Similarly, Hallstrand et al40 found that screening histories of identified subjects with symptoms or a previous diagnosis suggestive of EIB in 39.5% of the participants, but only 12.9% of these persons actually had EIB. Surprisingly, 7.8% of adolescents in that study with a globally negative review of symptoms of asthma or EIB actually had EIB. Holzer et al8 reported that only 60% of athletes with a positive result for an exercise challenge test reported symptoms. The lack of sensitivity and specificity of the history and physical examination in the evaluation of EIB requires the clinician to perform objective diagnostic testing when there is a suspicion of EIB.

Objective testing should begin with spirometry before and after inhaled bronchodilator therapy, which frequently will identify athletes who have abnormal baseline lung function. However, many athletes who are not asthmatic but who experience EIB will have will have normal baseline lung function.41In this cohort of athletes, spirometry alone is not adequate to diagnose EIB. Significant numbers of false-negative results may occur if adequate exercise and environmental stress is not provided in the evaluation for EIB. In athletes with normal findings on physical examination and spirometry, bronchoprovocation testing is recommended. A positive bronchoprovocation test result indicates a need for treatment for EIB. Objective change (usually a ≥ 10% decrease in FEV1) between pre-bronchoprovocation testing and post-bronchoprovocation testing values is necessary to confirm the diagnosis of EIB.42 If the athlete with persistent exercise-related symptoms has negative physical examination, spirometry, and bronchoprovocation testing results, we recommend reconsidering alternative diagnoses.

Various bronchoprovocation techniques exist; however, not all are equally valuable or accurate in assessing EIB in athletes. The International Olympic Committee adopted the eucapnic voluntary hyperventilation (EVH) challenge as the test recommended to document EIB in olympians.43EVH involves the hyperventilation of a gas mixture of 5% CO2 and 21% O2 at 85% of maximum voluntary ventilation for 6 min and the assessment of FEV1 at specified intervals after the test; this challenge test has been shown to have a high specificity44 for EIB. EVH has been shown to be more sensitive in some studies for detecting EIB than methacholine8 or field or laboratory-based exercise testing.4445 The test is portable, relatively inexpensive, and there are protocols46that allow standardization between laboratories. Mannix et al47 used EVH to screen 79 high school athletes and found that 38% of them had EIB. EVH is an extremely valuable bronchoprovocation technique given its sensitivity and specificity, portability, and standardization of protocol. It is possible that the increased sensitivity of EVH for detecting EIB will demonstrate prevalence rates in athletes that are higher than those previously reported.

Pharmacologic challenge tests, such as the methacholine or histamine challenge test, have been shown to have a lower sensitivity than EVH for the detection of EIB in elite athletes8 and are not recommended first-line tests for use in the evaluation of EIB in athletes. Holzer et al8 showed that of 42 elite athletes with respiratory symptoms, EVH detected 25 (60%) while methacholine challenge detected only 9 (21%).

A newer, promising technique involves the inhalation of mannitol in dry-powder form. Holzer et al48 studied 50 athletes and demonstrated that osmotic challenge testing with dry-powder mannitol challenge has both a high sensitivity and specificity for EIB. Mannitol had a sensitivity of 96% and a specificity of 92% to identify a positive response to EVH, and could be used as an alternative to EVH testing to identify EIB if EVH testing is not available. However, mannitol inhalation does not simulate exercise, and, currently, only one study has investigated its value in detecting EIB specifically in athletes.48

Pharmacologic therapy (Table 3 ) for EIB has been studied extensively; however, most studies have included asthmatic athletes, and there are no guidelines currently available to guide pharmacotherapy in nonasthmatic EIB patients. It is not known whether the recommended therapy for EIB in asthmatic athletes is as efficacious in nonasthmatic athletes who experience EIB.

The most common therapeutic recommendation for minimizing or preventing symptoms in athletes who have EIB is the prophylactic use of short-acting bronchodilators (ie, β2-receptor agonists) such as albuterol shortly before exercise. β2-agonists are considered to be the most effective therapy for the prevention of symptoms of EIB in asthmatic patients.37,49Treatment with two puffs of a short-acting β2-receptor agonists shortly before (15 min) exercise will provide peak bronchodilation in 15 to 60 min and protection from EIB for at least 3 h in most patients.50 However, the overuse of β2-agonists has been shown to result in tachyphylaxis and to worsen symptoms of EIB and asthma.,49

Long-acting bronchodilators work in a pharmacologically similar manner as short-acting bronchodilators. The bronchoprotection afforded by long-acting β2-receptor agonists has been shown to last up to 12 h,51whereas the effect of albuterol is no longer significant by 4 h.52Ferrari et al53demonstrated that the inhalation of formoterol, a long-acting β2-receptor agonist, is effective in protecting asthmatic athletes as early as 15 min after dosing. Furthermore, Ferrari et al54 compared the effects of formoterol vs salmeterol in preventing EIB and again found that formoterol was effective 15 min after dosing, but that salmeterol was not effective that rapidly. Both medications were equally effective at 4 h. In a study comparing the average onset of action of formoterol vs salmeterol, Palmqvist et al55found that formoterol was effective in approximately 12 min while salmeterol was effective after 31 min. The results of these studies suggest that there are differences in the pharmacokinetics between salmeterol and formoterol, and that administration of salmeterol should occur significantly in advance of exercise for it to be optimally effective in preventing EIB. It is also important to stress the fact that long-acting β2-receptor agonists in general are not rescue medications and should not be used more than twice a day. Tachyphylaxis also has been shown to occur after repeated use of long-acting β2-receptor agonists56; thus, close follow-up is recommended when using these medications.

Inhaled corticosteroids are recommended as first-line therapy in terms of controller medications for athletes who have asthma and experience EIB.26 Airway inflammation is also often present in nonasthmatic athletes who have EIB,30,57and, therefore, inhaled corticosteroids may be an effective medicine for treatment; however, the efficacy of corticosteroids in this cohort has not been studied. Thio et al58showed that a single high dose of inhaled fluticasone propionate had an acute protective effect on the bronchial response to exercise in a substantial proportion of asthmatic patients enrolled in the study. Similarly, Jonasson59 concluded that patients with mild asthma, but with significant EIB, improved their exercise tolerance and symptom control after 3 months of treatment with a low dose of inhaled budesonide administered once or twice daily.

Leukotriene modifiers have been shown to be effective in controlling patients with EIB.6064 Leukotriene modifiers have become an attractive therapy for EIB as a result of their efficacy, once-a-day dosing, and oral formulation. Leff et al65evaluated the ability of montelukast, a leukotriene-receptor antagonist, to protect patients against EIB. Montelukast therapy offered significantly greater protection against EIB than placebo therapy and was also associated with a significant improvement in the maximal decrease in FEV1 after exercise. In addition, tolerance to the medication and rebound worsening of lung function after the discontinuation of treatment were not seen. Rundell et al66 found that a single dose of montelukast provided reasonable protection in attenuating bronchoconstriction resulting from either exercise or EVH.

Leukotriene modifiers may be a more effective alternative in treating EIB than long-acting β2-receptor agonists. Villaran et al67evaluated 192 asthmatic patients with documented EIB and found that the effect of montelukast was greater than that of salmeterol in the long-term treatment of EIB over a period of 8 weeks in patients with mild asthma, as demonstrated by effect size, maintenance of the effect, and fewer respiratory clinical adverse events during the study period. Inhaled corticosteroids have been shown to be superior to leukotriene modifiers in managing chronic asthma.68 However, we are aware of no studies comparing these medications head-to-head in terms of their effectiveness in preventing EIB in athletes.

Mast cell stabilizers have been used extensively for the prophylaxis of EIB. These medications prevent mast cell degranulation and subsequent histamine release.69When a dose of either cromolyn or nedocromil has been administered to athletes 15 to 20 min prior to exercise, both agent have been shown to be effective in preventing EIB.7071 In a metaanalysis72 of the prevention of EIB in asthmatic patients, nedocromil sodium was found to improve FEV1 by an average of 16% and to shorten the duration of EIB symptoms to < 10 min. While these agents are effective, they are often used as a second-line agent due to their cost, and the fact that their duration of action and efficacy is less than that of β-agonists.

Multiple pharmacologic approaches can be employed in the same patient if necessary. Combination inhalers (eg, fluticasone/salmeterol) have been become popular as a result of their effectiveness and convenience. Weiler et al73showed that long-term fluticasone/salmeterol therapy provided protection against exercise-induced bronchospasm in patients with persistent asthma. Woolley et al74 demonstrated that athletes in their cohort had a longer duration of protection from a combination of short-acting β2-receptor agonists and cromolyn compounds than from either medication used as monotherapy.

Other less commonly used inhaled pharmacologic agents that have been shown to prevent EIB include heparin7576 and furosemide.7778 However, the sample sizes in these studies were small, and the effects of these medications need to be validated in larger studies.

Many athletes find that a period of precompetition warm-up reduces the symptoms of EIB that occur during their competitive activity. Athletes often draw this conclusion without any guidance from health-care specialists. Symptoms of EIB usually occur after a few minutes of exercise, and some athletes find that warming up before exercise acts as prophylaxis against more significant episodes of EIB during exercise. It has been shown by investigators that this phenomenon of the “refractory period” does occur in some athletes with asthma and that athletes can be refractory to an exercise task performed within 2 h of an exercise warm-up.7981 The refractory period is hypothesized to be secondary to the release of catecholamines such as epinephrine and norepinephrine, which are bronchodilators and to depletion of mast cell contents such as histamine which cause bronchoconstriction. However, the refractory period has not been consistently proven across different athletic populations and has not been well-documented in EIB-positive athletes who are not asthmatic.82

There are other nonpharmacologic strategies (Table 3) that athletes can employ to help reduce the frequency and severity of symptoms of EIB. Wearing a facemask during activity warms and humidifies inspired air when outdoor conditions are cold and dry, and is especially valuable to elite and recreational athletes who exercise in the winter.83Breathing through the nose rather than the mouth will also help to ameliorate EIB84 by warming, filtering, and humidifying the air, which subsequently reduces airway cooling and dehydration. In addition, athletes with knowledge of triggers (ie, freshly cut grass) should attempt to avoid them if possible.

In our experience, both pharmacologic and nonpharmacologic approaches are essential to minimizing the adverse effects of EIB. We recommend starting athletes that have clinical evidence of EIB on therapy with short-acting bronchodilators before exercise, and instructing them on the importance of adequate warm-up and avoidance of known triggers. This regimen will prevent significant EIB in > 80% of athletes.26 If symptoms persist, especially in athletes with asthma, inhaled corticosteroids should be added as maintenance therapy.26,5859 While the efficacy of therapy with inhaled steroids in nonasthmatic athletes has not been extensively evaluated, we recommend using them in nonasthmatic athletes whose symptoms are not completely controlled with short-acting bronchodilators, as there is evidence of increased inflammation, although not typical of classic asthma, in the airways of subjects without known asthma as a result of hyperventilation and exercise.2930 Alternatively, leukotriene modifiers65 or cromolyn compounds26,7071 can be used in athletes whose asthma is inadequately controlled with β2-agonists.

EIB in athletes is a problem that is likely more prevalent than currently clinically recognized. The consequences of misdiagnosis or the failure to diagnose entirely can result in the impairment of performance and can be detrimental to health. The cohort of athletes who experience EIB but are not asthmatic needs further study. There are many unanswered questions about the pathogenesis of EIB in this cohort and whether therapy targeted at EIB in asthmatic patients is as effective in nonasthmatic athletes who experience EIB. Physicians and trainers must have a high index of suspicion when healthy athletes complain of symptoms during exercise. Most importantly, the education of both athletes and health-care providers, in terms of recognition of an impending or ongoing episode of EIB and appropriate treatment for such an episode, is paramount.

Abbreviations: EIB = exercise-induced bronchoconstriction; EVH = eucapnic voluntary hyperventilation; NO = nitric oxide

Learning objectives: 1) Identify the most common trigger of bronchospasms in individuals known to be asthmatic. 2) List the most common clinical manifestations of exercise-induced bronchoconstriction. 3) State the most established diagnostic indicator of exercise-induced bronchoconstriction. 4) Indicate preventative methods that should be considered by those individuals who participate in organized sports who are also known asthmatics.

The following authors have disclosed financial relationships with a commercial party. Grant information and company names appear as provided by the presenter: Jonathan P. Parsons, MD: GlaxoSmithKline: Speaker bureau; The CHEST Foundation: $10,000 grant (from sources other than industry). John G. Mastronarde, MD, FCCP: GlaxoSmithKline: Speaker bureau.

Table Graphic Jump Location
Table 1. Prevalence of EIB
Table Graphic Jump Location
Table 2. Examples of High-Ventilation and Low-Ventilation Sports
Table Graphic Jump Location
Table 3. Management Strategies of EIB
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Leuppi, JD, Kuhn, M, Comminot, C, et al High prevalence of bronchial hyperresponsiveness and asthma in ice hockey players.Eur Respir J1998;12,13-16. [CrossRef] [PubMed]
 
Godfrey.. Clinical variables of exercise-induced bronchospasm. Dempsey, J eds.Muscular exercise and the lung1977,247-288 The University of Wisconsin Press. Madison, WI:
 
Brudno, DS, Wagner, JM, Rupp, NT Length of postexercise assessment in the determination of exercise-induced bronchospasm.Ann Allergy1994;73,227-231. [PubMed]
 
London, SJ, James, GW, Avol, E, et al Family history and the risk of early-onset persistent, early-onset transient, and late-onset asthma.Epidemiology2001;12,577-583. [CrossRef] [PubMed]
 
Hallstrand, TS, Curtis, JR, Koepsell, TD, et al Effectiveness of screening examinations to detect unrecognized exercise-induced bronchoconstriction.J Pediatr2002;141,343-348. [CrossRef] [PubMed]
 
Rundell, KW, Wilber, RL, Szmedra, L, et al Exercise-induced asthma screening of elite athletes: field versus laboratory exercise challenge.Med Sci Sports Exerc2000;32,309-316. [CrossRef] [PubMed]
 
Anderson, SD, Argyros, GJ, Magnussen, H, et al Provocation by eucapnic voluntary hyperpnoea to identify exercise induced bronchoconstriction.Br J Sports Med2001;35,344-347. [CrossRef] [PubMed]
 
International Olympic Committee. β.2 adrenoceptor agonists and the Olympic Games in Athens. Available at: http://multimedia.olympic.org/pdf/en report 732.pdf. Accessed September 1, 2004.
 
Eliasson, AH, Phillips, YY, Rajagopal, KR, et al Sensitivity and specificity of bronchial provocation testing: an evaluation of four techniques in exercise-induced bronchospasm.Chest1992;102,347-355. [CrossRef] [PubMed]
 
Rundell, KW, Anderson, SD, Spiering, BA, et al Field exercise vs laboratory eucapnic voluntary hyperventilation to identify airway hyperresponsiveness in elite cold weather athletes.Chest2004;125,909-915. [CrossRef] [PubMed]
 
Argyros, GJ, Roach, JM, Hurwitz, KM, et al Eucapnic voluntary hyperventilation as a bronchoprovocation technique: development of a standardized dosing schedule in asthmatics.Chest1996;109,1520-1524. [CrossRef] [PubMed]
 
Mannix, ET, Roberts, MA, Dukes, HJ, et al Airways hyperresponsiveness in high school athletes.J Asthma2004;41,567-574. [CrossRef] [PubMed]
 
Holzer, K, Anderson, SD, Chan, HK, et al Mannitol as a challenge test to identify exercise-induced bronchoconstriction in elite athletes.Am J Respir Crit Care Med2003;167,534-537. [CrossRef] [PubMed]
 
National Asthma Education and Prevention Program. Expert panel report: guidelines for the diagnosis and management of asthma update on selected topics; 2002.2002;110,S141-S219
 
Bierman, CW, Spiro, SG, Petheram, I Characterization of the late response in exercise-induced asthma.J Allergy Clin Immunol1984;74,701-706. [CrossRef] [PubMed]
 
Bronsky, EA YU, Yeh, CM, Larsen, LV, et al Formoterol provides long-lasting protection against exercise-induced bronchospasm.Ann Allergy Asthma Immunol2002;89,407-412. [CrossRef] [PubMed]
 
Shapiro, GS, Yegen, U, Xiang, J, et al A randomized, double-blind, single-dose, crossover clinical trial of the onset and duration of protection from exercise-induced bronchoconstriction by formoterol and albuterol.Clin Ther2002;24,2077-2087. [CrossRef] [PubMed]
 
Ferrari, M, Balestreri, F, Baratieri, S, et al Evidence of the rapid protective effect of formoterol dry-powder inhalation against exercise-induced bronchospasm in athletes with asthma.Respiration2000;67,510-513. [CrossRef] [PubMed]
 
Ferrari, MSC, Zanon, R, Bertaiola, M, et al Comparison of the protective effect of formoterol and of salmeterol against exercise-induced bronchospasm when given immediately before a cycloergometric test.Respiration2002;69,509-512. [CrossRef] [PubMed]
 
Palmqvist, MPG, Lazer, L, Rosenborg, J, et al Inhaled dry-powder formoterol and salmeterol in asthmatic patients: onset of action, duration of effect and potency.Eur Respir J1997;10,2484-2489. [CrossRef] [PubMed]
 
Coreno, A, Skowronski, M, Kotaru, C, et al Comparative effects of long-acting β2-agonists, leukotriene receptor antagonists, and a 5-lipoxygenase inhibitor on exercise-induced asthma.J Allergy Clin Immunol2000;106,500-506. [CrossRef] [PubMed]
 
Helenius, IJ, Rytila, P, Metso, T, et al Respiratory symptoms, bronchial responsiveness, and cellular characteristics of induced sputum in elite swimmers.Allergy1998;53,346-352. [CrossRef] [PubMed]
 
Thio, BJ, Slingerland, GL, Nagelkerke, AF, et al Effects of single-dose fluticasone on exercise-induced asthma in asthmatic children: a pilot study.Pediatr Pulmonol2001;32,115-121. [CrossRef] [PubMed]
 
Jonasson, G, Carlsen, KH, Hultquist, C Low-dose budesonide improves exercise-induced bronchospasm in schoolchildren.Pediatr Allergy Immunol2000;11,120-125. [CrossRef] [PubMed]
 
Kim, JH LS, Kim, HB, Kim, BS, et al Prolonged effect of montelukast in asthmatic children with exercise-induced bronchoconstriction.Pediatr Pulmonol2005;39,162-166. [CrossRef] [PubMed]
 
Dahlen, B, Roquet, A, Inman, MD, et al Influence of zafirlukast and loratadine on exercise-induced bronchoconstriction.J Allergy Clin Immunol2002;109,789-793. [CrossRef] [PubMed]
 
Dessanges, JF, Prefaut, C, Taytard, A, et al The effect of zafirlukast on repetitive exercise-induced bronchoconstriction: the possible role of leukotrienes in exercise-induced refractoriness.J Allergy Clin Immunol1999;104,1155-1161. [CrossRef] [PubMed]
 
Griffin, M, Weiss, JW, Leitch, AG, et al Effects of leukotriene D on the airways in asthma.N Engl J Med1983;308,436-439. [CrossRef] [PubMed]
 
Sin, DD, Man, J, Sharpe, H, et al Pharmacological management to reduce exacerbations in adults with asthma: a systematic review and meta-analysis.JAMA2004;292,367-376. [CrossRef] [PubMed]
 
Leff, JA, Busse, WW, Pearlman, D, et al Montelukast, a leukotriene-receptor antagonist, for the treatment of mild asthma and exercise-induced bronchoconstriction.N Engl J Med1998;339,147-152. [CrossRef] [PubMed]
 
Rundell, KW, Spiering, BA, Baumann, JM, et al Effect of montelukast on airway narrowing from eucapnic voluntary hyperventilation and cold air exercise.Br J Sports Med2005;39,232-236. [CrossRef] [PubMed]
 
Villaran, C, O’Neill, SJ, Helbling, A, et al Montelukast versus salmeterol in patients with asthma and exercise-induced bronchoconstriction: Montelukast/Salmeterol Exercise Study Group.J Allergy Clin Immunol1999;104,547-553. [CrossRef] [PubMed]
 
Ng DSF, Hicks G. Anti-leukotriene agents compared to inhaled corticosteroids in the management of recurrent and/or chronic asthma in adults and children. Cochrane Database Syst Rev (database online). Issue 2, 2004.
 
The Medical Letter, Inc.. Drugs for asthma.Med Lett Drugs Ther2000;42,19-24. [PubMed]
 
Albazzaz, MK, Neale, MG, Patel, KR Dose duration of nebulized nedocromil sodium in exercise-induced asthma.Eur Respir J1992;5,967-969. [PubMed]
 
de Benedictis, FM, Tuteri, G, Pazzelli, P, et al Cromolyn versus nedocromil: duration of action in exercise-induced asthma in children.J Allergy Clin Immunol1995;96,510-514. [CrossRef] [PubMed]
 
Kelly K, Spooner CH, Rowe BH. Nedocromil sodium vs. sodium cromoglycate for preventing exercise-induced bronchoconstriction in asthmatics. Cochrane Database Syst Rev (database online). Issue 4, 2000.
 
Weiler, JM NR, Rupp, NT, Kalberg, CJ, et al Effect of fluticasone/salmeterol administered via a single device on exercise-induced bronchospasm in patients with persistent asthma.Ann Allergy Asthma Immunol2005;94,65-72. [CrossRef] [PubMed]
 
Woolley, M, Anderson, SD, Quigley, BM Duration of protective effect of terbutaline sulfate and cromolyn sodium alone and in combination on exercise-induced asthma.Chest1990;97,39-45. [CrossRef] [PubMed]
 
Garrigo, J, Danta, I, Ahmed, T Time course of the protective effect of inhaled heparin on exercise-induced asthma.Am J Respir Crit Care Med1996;153,1702-1707. [PubMed]
 
Ahmed, T, Garrigo, J, Danta, I Preventing bronchoconstriction in exercise-induced asthma with inhaled heparin.N Engl J Med1993;329,90-95. [CrossRef] [PubMed]
 
Munyard, P, Chung, KF, Bush, A Inhaled frusemide and exercise-induced bronchoconstriction in children with asthma.Thorax1995;50,677-679. [CrossRef] [PubMed]
 
Novembre, E, Frongia, G, Lombardi, E, et al The preventive effect and duration of action of two doses of inhaled furosemide on exercise-induced asthma in children.J Allergy Clin Immunol1995;96,906-909. [CrossRef] [PubMed]
 
Anderson, SD, Schoeffel, RE Respiratory heat and water loss during exercise in patients with asthma: effect of repeated exercise challenge.Eur J Respir Dis1982;63,472-480. [PubMed]
 
McKenzie, DC, McLuckie, SL, Stirling, DR The protective effects of continuous and interval exercise in athletes with exercise-induced asthma.Med Sci Sports Exerc1994;26,951-956. [PubMed]
 
Schnall, RP, Landau, LI Protective effects of repeated short sprints in exercise-induced asthma.Thorax1980;35,828-832. [CrossRef] [PubMed]
 
Rundell, KW, Spiering, BA, Judelson, DA, et al Bronchoconstriction during cross-country skiing: is there really a refractory period?Med Sci Sports Exerc2003;35,18-26. [CrossRef] [PubMed]
 
Schacter, E The protective effects of a cold weather mask on EIA.Ann Allergy1982;,12-16
 
Shturman-Ellstein, RZR, Buckley, JM, Souhrada, JF The beneficial effect of nasal breathing on exercise-induced bronchoconstriction.Am Rev Respir Dis1978;118,65-73. [PubMed]
 
Provost-Craig, MA, Arbour, KS, Sestili, DC, et al The incidence of exercise-induced bronchospasm in competitive figure skaters.J Asthma1996;33,67-71. [CrossRef] [PubMed]
 

Tables

Table Graphic Jump Location
Table 1. Prevalence of EIB
Table Graphic Jump Location
Table 2. Examples of High-Ventilation and Low-Ventilation Sports
Table Graphic Jump Location
Table 3. Management Strategies of EIB

References

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Eggleston, PA, Kagey-Sobotka, A, Lichtenstein, LM A comparison of the osmotic activation of basophils and human lung mast cells.Am Rev Respir Dis1987;135,1043-1048. [PubMed]
 
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National Asthma Education and Prevention Program.. Expert panel report 2: guidelines for the diagnosis and management of asthma.April 1997,97-4051 National Institutes of Health. Bethesda, MD:
 
Koh, YI, Choi, S Blood eosinophil counts for the prediction of the severity of exercise-induced bronchospasm in asthma.Respir Med2002;96,120-125. [CrossRef] [PubMed]
 
Otani, K, Kanazawa, H, Fujiwara, H, et al Determinants of the severity of exercise-induced bronchoconstriction in patients with asthma.J Asthma2004;41,271-278. [CrossRef] [PubMed]
 
Karjalainen, EM, Laitinen, A, Sue-Chu, M, et al Evidence of airway inflammation and remodeling in ski athletes with and without bronchial hyperresponsiveness to methacholine.Am J Respir Crit Care Med2000;161,2086-2091. [PubMed]
 
Larsson, K, Tornling, G, Gavhed, D, et al Inhalation of cold air increases the number of inflammatory cells in the lungs in healthy subjects.Eur Respir J1998;12,825-830. [CrossRef] [PubMed]
 
Davis, MS, Freed, AN Repetitive hyperpnoea causes peripheral airway obstruction and eosinophilia.Eur Respir J1999;14,57-62. [CrossRef] [PubMed]
 
Kotaru, C, Coreno, A, Skowronski, M, et al Exhaled nitric oxide and thermally induced asthma.Am J Respir Crit Care Med2001;163,383-388. [PubMed]
 
Holzer, K, Brukner, P Screening of athletes for exercise-induced bronchoconstriction.Clin J Sport Med2004;14,134-138. [CrossRef] [PubMed]
 
Helenius, I, Haahtela, T Allergy and asthma in elite summer sport athletes.J Allergy Clin Immunol2000;106,444-452. [CrossRef] [PubMed]
 
Brauer, M, Spengler, JD Nitrogen dioxide exposures inside ice skating rinks.Am J Public Health1994;84,429-433. [CrossRef] [PubMed]
 
Leuppi, JD, Kuhn, M, Comminot, C, et al High prevalence of bronchial hyperresponsiveness and asthma in ice hockey players.Eur Respir J1998;12,13-16. [CrossRef] [PubMed]
 
Godfrey.. Clinical variables of exercise-induced bronchospasm. Dempsey, J eds.Muscular exercise and the lung1977,247-288 The University of Wisconsin Press. Madison, WI:
 
Brudno, DS, Wagner, JM, Rupp, NT Length of postexercise assessment in the determination of exercise-induced bronchospasm.Ann Allergy1994;73,227-231. [PubMed]
 
London, SJ, James, GW, Avol, E, et al Family history and the risk of early-onset persistent, early-onset transient, and late-onset asthma.Epidemiology2001;12,577-583. [CrossRef] [PubMed]
 
Hallstrand, TS, Curtis, JR, Koepsell, TD, et al Effectiveness of screening examinations to detect unrecognized exercise-induced bronchoconstriction.J Pediatr2002;141,343-348. [CrossRef] [PubMed]
 
Rundell, KW, Wilber, RL, Szmedra, L, et al Exercise-induced asthma screening of elite athletes: field versus laboratory exercise challenge.Med Sci Sports Exerc2000;32,309-316. [CrossRef] [PubMed]
 
Anderson, SD, Argyros, GJ, Magnussen, H, et al Provocation by eucapnic voluntary hyperpnoea to identify exercise induced bronchoconstriction.Br J Sports Med2001;35,344-347. [CrossRef] [PubMed]
 
International Olympic Committee. β.2 adrenoceptor agonists and the Olympic Games in Athens. Available at: http://multimedia.olympic.org/pdf/en report 732.pdf. Accessed September 1, 2004.
 
Eliasson, AH, Phillips, YY, Rajagopal, KR, et al Sensitivity and specificity of bronchial provocation testing: an evaluation of four techniques in exercise-induced bronchospasm.Chest1992;102,347-355. [CrossRef] [PubMed]
 
Rundell, KW, Anderson, SD, Spiering, BA, et al Field exercise vs laboratory eucapnic voluntary hyperventilation to identify airway hyperresponsiveness in elite cold weather athletes.Chest2004;125,909-915. [CrossRef] [PubMed]
 
Argyros, GJ, Roach, JM, Hurwitz, KM, et al Eucapnic voluntary hyperventilation as a bronchoprovocation technique: development of a standardized dosing schedule in asthmatics.Chest1996;109,1520-1524. [CrossRef] [PubMed]
 
Mannix, ET, Roberts, MA, Dukes, HJ, et al Airways hyperresponsiveness in high school athletes.J Asthma2004;41,567-574. [CrossRef] [PubMed]
 
Holzer, K, Anderson, SD, Chan, HK, et al Mannitol as a challenge test to identify exercise-induced bronchoconstriction in elite athletes.Am J Respir Crit Care Med2003;167,534-537. [CrossRef] [PubMed]
 
National Asthma Education and Prevention Program. Expert panel report: guidelines for the diagnosis and management of asthma update on selected topics; 2002.2002;110,S141-S219
 
Bierman, CW, Spiro, SG, Petheram, I Characterization of the late response in exercise-induced asthma.J Allergy Clin Immunol1984;74,701-706. [CrossRef] [PubMed]
 
Bronsky, EA YU, Yeh, CM, Larsen, LV, et al Formoterol provides long-lasting protection against exercise-induced bronchospasm.Ann Allergy Asthma Immunol2002;89,407-412. [CrossRef] [PubMed]
 
Shapiro, GS, Yegen, U, Xiang, J, et al A randomized, double-blind, single-dose, crossover clinical trial of the onset and duration of protection from exercise-induced bronchoconstriction by formoterol and albuterol.Clin Ther2002;24,2077-2087. [CrossRef] [PubMed]
 
Ferrari, M, Balestreri, F, Baratieri, S, et al Evidence of the rapid protective effect of formoterol dry-powder inhalation against exercise-induced bronchospasm in athletes with asthma.Respiration2000;67,510-513. [CrossRef] [PubMed]
 
Ferrari, MSC, Zanon, R, Bertaiola, M, et al Comparison of the protective effect of formoterol and of salmeterol against exercise-induced bronchospasm when given immediately before a cycloergometric test.Respiration2002;69,509-512. [CrossRef] [PubMed]
 
Palmqvist, MPG, Lazer, L, Rosenborg, J, et al Inhaled dry-powder formoterol and salmeterol in asthmatic patients: onset of action, duration of effect and potency.Eur Respir J1997;10,2484-2489. [CrossRef] [PubMed]
 
Coreno, A, Skowronski, M, Kotaru, C, et al Comparative effects of long-acting β2-agonists, leukotriene receptor antagonists, and a 5-lipoxygenase inhibitor on exercise-induced asthma.J Allergy Clin Immunol2000;106,500-506. [CrossRef] [PubMed]
 
Helenius, IJ, Rytila, P, Metso, T, et al Respiratory symptoms, bronchial responsiveness, and cellular characteristics of induced sputum in elite swimmers.Allergy1998;53,346-352. [CrossRef] [PubMed]
 
Thio, BJ, Slingerland, GL, Nagelkerke, AF, et al Effects of single-dose fluticasone on exercise-induced asthma in asthmatic children: a pilot study.Pediatr Pulmonol2001;32,115-121. [CrossRef] [PubMed]
 
Jonasson, G, Carlsen, KH, Hultquist, C Low-dose budesonide improves exercise-induced bronchospasm in schoolchildren.Pediatr Allergy Immunol2000;11,120-125. [CrossRef] [PubMed]
 
Kim, JH LS, Kim, HB, Kim, BS, et al Prolonged effect of montelukast in asthmatic children with exercise-induced bronchoconstriction.Pediatr Pulmonol2005;39,162-166. [CrossRef] [PubMed]
 
Dahlen, B, Roquet, A, Inman, MD, et al Influence of zafirlukast and loratadine on exercise-induced bronchoconstriction.J Allergy Clin Immunol2002;109,789-793. [CrossRef] [PubMed]
 
Dessanges, JF, Prefaut, C, Taytard, A, et al The effect of zafirlukast on repetitive exercise-induced bronchoconstriction: the possible role of leukotrienes in exercise-induced refractoriness.J Allergy Clin Immunol1999;104,1155-1161. [CrossRef] [PubMed]
 
Griffin, M, Weiss, JW, Leitch, AG, et al Effects of leukotriene D on the airways in asthma.N Engl J Med1983;308,436-439. [CrossRef] [PubMed]
 
Sin, DD, Man, J, Sharpe, H, et al Pharmacological management to reduce exacerbations in adults with asthma: a systematic review and meta-analysis.JAMA2004;292,367-376. [CrossRef] [PubMed]
 
Leff, JA, Busse, WW, Pearlman, D, et al Montelukast, a leukotriene-receptor antagonist, for the treatment of mild asthma and exercise-induced bronchoconstriction.N Engl J Med1998;339,147-152. [CrossRef] [PubMed]
 
Rundell, KW, Spiering, BA, Baumann, JM, et al Effect of montelukast on airway narrowing from eucapnic voluntary hyperventilation and cold air exercise.Br J Sports Med2005;39,232-236. [CrossRef] [PubMed]
 
Villaran, C, O’Neill, SJ, Helbling, A, et al Montelukast versus salmeterol in patients with asthma and exercise-induced bronchoconstriction: Montelukast/Salmeterol Exercise Study Group.J Allergy Clin Immunol1999;104,547-553. [CrossRef] [PubMed]
 
Ng DSF, Hicks G. Anti-leukotriene agents compared to inhaled corticosteroids in the management of recurrent and/or chronic asthma in adults and children. Cochrane Database Syst Rev (database online). Issue 2, 2004.
 
The Medical Letter, Inc.. Drugs for asthma.Med Lett Drugs Ther2000;42,19-24. [PubMed]
 
Albazzaz, MK, Neale, MG, Patel, KR Dose duration of nebulized nedocromil sodium in exercise-induced asthma.Eur Respir J1992;5,967-969. [PubMed]
 
de Benedictis, FM, Tuteri, G, Pazzelli, P, et al Cromolyn versus nedocromil: duration of action in exercise-induced asthma in children.J Allergy Clin Immunol1995;96,510-514. [CrossRef] [PubMed]
 
Kelly K, Spooner CH, Rowe BH. Nedocromil sodium vs. sodium cromoglycate for preventing exercise-induced bronchoconstriction in asthmatics. Cochrane Database Syst Rev (database online). Issue 4, 2000.
 
Weiler, JM NR, Rupp, NT, Kalberg, CJ, et al Effect of fluticasone/salmeterol administered via a single device on exercise-induced bronchospasm in patients with persistent asthma.Ann Allergy Asthma Immunol2005;94,65-72. [CrossRef] [PubMed]
 
Woolley, M, Anderson, SD, Quigley, BM Duration of protective effect of terbutaline sulfate and cromolyn sodium alone and in combination on exercise-induced asthma.Chest1990;97,39-45. [CrossRef] [PubMed]
 
Garrigo, J, Danta, I, Ahmed, T Time course of the protective effect of inhaled heparin on exercise-induced asthma.Am J Respir Crit Care Med1996;153,1702-1707. [PubMed]
 
Ahmed, T, Garrigo, J, Danta, I Preventing bronchoconstriction in exercise-induced asthma with inhaled heparin.N Engl J Med1993;329,90-95. [CrossRef] [PubMed]
 
Munyard, P, Chung, KF, Bush, A Inhaled frusemide and exercise-induced bronchoconstriction in children with asthma.Thorax1995;50,677-679. [CrossRef] [PubMed]
 
Novembre, E, Frongia, G, Lombardi, E, et al The preventive effect and duration of action of two doses of inhaled furosemide on exercise-induced asthma in children.J Allergy Clin Immunol1995;96,906-909. [CrossRef] [PubMed]
 
Anderson, SD, Schoeffel, RE Respiratory heat and water loss during exercise in patients with asthma: effect of repeated exercise challenge.Eur J Respir Dis1982;63,472-480. [PubMed]
 
McKenzie, DC, McLuckie, SL, Stirling, DR The protective effects of continuous and interval exercise in athletes with exercise-induced asthma.Med Sci Sports Exerc1994;26,951-956. [PubMed]
 
Schnall, RP, Landau, LI Protective effects of repeated short sprints in exercise-induced asthma.Thorax1980;35,828-832. [CrossRef] [PubMed]
 
Rundell, KW, Spiering, BA, Judelson, DA, et al Bronchoconstriction during cross-country skiing: is there really a refractory period?Med Sci Sports Exerc2003;35,18-26. [CrossRef] [PubMed]
 
Schacter, E The protective effects of a cold weather mask on EIA.Ann Allergy1982;,12-16
 
Shturman-Ellstein, RZR, Buckley, JM, Souhrada, JF The beneficial effect of nasal breathing on exercise-induced bronchoconstriction.Am Rev Respir Dis1978;118,65-73. [PubMed]
 
Provost-Craig, MA, Arbour, KS, Sestili, DC, et al The incidence of exercise-induced bronchospasm in competitive figure skaters.J Asthma1996;33,67-71. [CrossRef] [PubMed]
 
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