Exercise-induced bronchospasm (EIB) describes airway narrowing that occurs in association with exercise. The airway obstruction associated with exercise commonly occurs after exercise has ceased. Exercise is one of the most common triggers of bronchospasm in patients with chronic asthma, and EIB occurs in 80-90% of individuals with known asthma (17). EIB also occurs in approximately 10% of the general population who do not have a known history of chronic asthma (6). These patients have symptoms of asthma only when they exercise.
The prevalence of EIB in elite, Olympic athletes has been reported to be as much as five times greater than that of the general population (19,25). However, there have been relatively few studies investigating the prevalence of EIB specifically in college athletes (10,22,27). This population is of particular interest, because many of the reported severe episodes of asthma provoked by exercise that have led to morbidity and mortality have occurred in competitive athletes that were less than 21 yr of age (4). Furthermore, prior studies of college athletes did not use eucapnic voluntary hyperpnea (EVH) as a bronchoprovocation technique, which has been shown to be a sensitive test for diagnosing EIB (7,14-16). The International Olympic Committee considers EVH to be the bronchoprovocation test of choice to document EIB (2), and EVH has been shown to be superior in diagnosing EIB compared with methacholine or traditional exercise challenges (7,23).
The specific aim of this study was to investigate the prevalence of EIB in a cohort of varsity athletes at The Ohio State University using eucapnic voluntary hyperpnea as a bronchoprovocation technique. We also examined whether there were interactions between the prevalence of EIB and presence of subjective respiratory symptoms, the type of sport (high ventilation vs low ventilation) in which the athlete participated, or the sex of the athlete. We hypothesized that there would be a significant prevalence of EIB in this cohort of college athletes, even in those with no history of asthma, after EVH challenge testing.
Potential participants in the study were members of male and female varsity athletic teams at The Ohio State University. Exclusion criteria included pregnancy, recent upper-respiratory tract infection (within 2 wk of study enrollment), a history of > 10 pack-years of tobacco use (calculated by multiplying the number of packs of cigarettes smoked per day by the number of years the person has smoked), or history of asthma with a current forced expiratory volume in 1 s (FEV1) of less than 70% of the predicted value on baseline spirometry, which would identify airway obstruction and possibly poor asthma control. A history of asthma was defined as a prior diagnosis of asthma by a physician.
Study design and protocol.
Varsity athletes were recruited on two separate occasions at mandatory preparticipation screening physicals at The Ohio State University. Athletes were presented the proposal in a short oral presentation and then given the opportunity to participate in the trial. All participation was voluntary and written informed consent was obtained from every participant prior to enrollment. The study received the approval of the institutional review board at The Ohio State University and the National Collegiate Athletic Association Compliance Office.
Participation in the study required two visits (Fig. 1). At the first visit, athletes underwent baseline spirometry following American Thoracic Society (ATS) guidelines (18) and completed a questionnaire addressing respiratory symptoms (e.g., wheezing, dyspnea, chest pain) during exercise designed by the U. S. Olympic Committee Sports Medicine Division (28). At the second visit, athletes underwent eucapnic voluntary hyperpnea bronchoprovocation testing using the method of Anderson et al. (1).
Each athlete performed baseline spirometry according to ATS standards (18). EVH bronchoprovocation challenge testing was then performed after spirometry. Participants breathed a mixture of dry compressed gas (5.0% CO2, 21.0% O2, balance N2) at a target rate of 85% of their maximum voluntary ventilation (MVV) per minute (calculated as 30 times the baseline FEV1, which approximates 85% MVV) for 6 min. Gas was channeled from a cylinder into a calibrated Rotometer (Brooks Model 1307) and then through an inspiratory target balloon (medical research bladder 100 MRL) that was maintained half full (to ensure correct minute ventilation) and then to a two-way, low-resistance valve (Hans Rudolph, Model 2700 2-Way Non-Rebreathing Valve) and mouthpiece (Medical Graphics #758301-001) for exercise. A metronome, timed for 30 cycles per minute, was used to help guide the athlete to achieve their target MVV. Spirometry was performed at 3, 5, 10, 15, and 20 min after the EVH challenge.
Criteria for diagnosis of EIB.
An EVH test was defined by a decline post-EVH testing of any of the following: FEV1 of > 10%, forced vital capacity (FVC) > 5%, or peak expiratory flow rate (PEFR) > 20% (11).
Measurements and statistical methods.
The primary aim of this study was to determine the prevalence of exercise-induced bronchospasm in a cohort of college athletes. The interaction of type of sport, sex of the athlete and presence of symptoms was also analyzed. Pearson's chi-square and logistic regression coefficients were used to test the significance of these associations. Significance was defined as a P value < 0.05. Sports were subjectively defined as high or low ventilation according to the ventilatory demands required to compete in the sport (29). All statistical analyses were run using Stata/SE, version 9.2, College Station, TX.
One hundred seven athletes from 22 different varsity sports completed both visits. Overall, participants were young, healthy, free of comorbidities, predominantly Caucasian, and had normal lung function (Table 1). No athlete that consented for participation was excluded on the basis of any of the exclusion criteria.
Eleven athletes had a history of asthma. All athletes, including the 11 athletes with a history of asthma, had normal spirometry at rest and were able to meet ATS standards for FVC measurement. Forty-two of 107 athletes (39%) had positive EVH tests indicating EIB (Table 2). Sixteen of 22 sports represented in the trial had at least one EIB-positive athlete. Of the 42 EIB-positive athletes, 36 (86%) had no prior known history of asthma or EIB. Only 3 of 107 athletes were on any type of asthma medication, and all three were EIB positive.
In the subgroup of athletes who had a prior history of asthma or EIB, 6 of 11 (55%) were EIB positive after EVH challenge. Post-EVH pulmonary function data for all athletes is shown in Table 3. All athletes reached their target minute ventilation rates. Athletes were analyzed according to participation in sports that are traditionally considered high ventilation versus low ventilation (Fig. 2) (29). High-ventilation sports require sustained periods of high aerobic and ventilatory demand (i.e., soccer, lacrosse). Twenty-nine of 71 athletes (41%) who participated in high-ventilation sports were EIB positive versus 13 of 36 athletes (36%) who played low-ventilation sports (95% confidence interval (CI) 0.53-2.79, odds ratio (OR) 1.22, P = 0.64).
The prevalence of EIB was not affected by the sex of the athlete. Female athletes had a prevalence of EIB of 42% compared with 38% of male athletes (CI 0.36-1.90, P = 0.65). Logistic regression of EIB status on ventilation and sex demonstrated an odds ratio of 2.1 for EIB in high-ventilation sports (CI 0.59-7.5, P = 0.25) and 0.47 for EIB for male sex (CI 0.13-1.7, P = 0.26).
The presence of symptoms did not predict whether athletes were EIB positive. The prevalence of EIB was 36% in athletes with negative symptoms and 35% for those with positive symptoms. Forty-eight percent of athletes who participated in high-ventilation sports had symptoms suggestive of EIB, which was significantly greater when compared with 25% of athletes in low-ventilation sports (P = 0.02); however, there was no difference in the prevalence of EIB between the groups (P = 0.64). There was no significant difference in the presence of symptoms between males (41%) and females (39%).
We report the first data on the prevalence of EVH-defined EIB in varsity college athletes. Currently, the International Olympic Committee considers EVH to be the bronchoprovocation test of choice to document EIB (2). This is the first study that applies the methodology that the International Olympic Committee recommends for diagnosis of EIB to college athletes. The high prevalence of EIB in our population (39%) is consistent with previously reported data investigating EIB in college athletes using alternative bronchoprovocation techniques (22,27).
Our results are also consistent with previous studies that have reported a poor correlation between symptoms and objectively proven EIB in athletes (8,12,24). In our study, fewer than half of all athletes who reported symptoms were EIB positive. The poor predictive value of symptoms was further demonstrated by finding that athletes who participate in high-ventilation sports were significantly more symptomatic than athletes in low-ventilation sports; however, there was no significant difference in objectively documented EIB between these groups. The wide variation in the reported prevalence of EIB in other studies may be related in part to this poor correlation between subjective symptoms and objective confirmation of EIB. Some studies of EIB have reported prevalence rates according to subjective symptoms alone (26); consequently, reported prevalence rates may be inaccurate, particularly in high-ventilation sports, because many athletes who do not undergo testing may be inaccurately diagnosed with EIB. These data have particular clinical relevance because physicians commonly diagnose and treat suspected EIB empirically according to symptoms alone, without objective testing (20); these results also suggest that objective testing should be performed when EIB is suspected, especially in athletes.
Although the nonspecific nature of symptoms can lead to an overdiagnosis of EIB, they can also lead to missed diagnoses of EIB, because symptoms may be mistaken for exertional fatigue, lack of conditioning, or lack of motivation in athletes who are truly EIB positive. As a result, many athletes with EIB may be unrecognized. Twenty-seven of 107 athletes (25%) in our study did not report symptoms during exercise but were found to have EIB. Asthmatics have been documented to be poor perceivers of bronchospasm (3). It is possible that a similar phenomenon occurs in nonasthmatic athletes, because absence of reported symptoms has been shown to be inadequate to exclude EIB in nonasthmatic athletes (24). This population of "silent EIB" may be at increased risk for morbidity from undiagnosed and untreated EIB. This is especially relevant in college athletes because a significant percentage of severe episodes of asthma related to exercise have been reported in athletes who have been younger than 21 yr of age (4). Objective testing likely would reduce the number of inaccurate diagnoses of EIB that are made on the basis of symptoms alone, as well as the number of missed diagnoses that could occur as a result of attributing EIB to normal manifestations of intense exercise. Furthermore, data also suggest that identifying young, asymptomatic athletes with EIB is important, because EIB in childhood and adolescence may predict the subsequent development of asthma in adulthood (21). Hence, finding an EIB-positive athlete who does not report symptoms may be of significant clinical relevance.
We found no significant difference in the prevalence of EIB between male and female athletes. This is in contrast to other studies that suggest the sex of the athlete may influence pulmonary function in athletes. Wilber et al. (30) found a statistically higher prevalence of EIB in female Winter Olympic athletes after exercise challenge compared with males. Previous studies also suggest that female athletes identify symptoms suggestive of EIB more often than male athletes during exercise (28). We also did not find a significant difference in the presence of symptoms between males and females.
Our data show no significant difference in the prevalence of EIB between athletes in high- versus low-ventilation sports. EIB has been thought to have a higher prevalence in endurance events such as cross-country skiing, swimming, and long-distance running, in which ventilation is increased for long periods of time during training and competition (8). Our results may have been influenced by the fact that we had significantly fewer athletes in low-ventilation sports who participated in the study, and by the small sample sizes in the individual sports.
The bronchoprovocation technique used to document EIB likely influences the variable prevalence of EIB reported in the literature. There remains an absence of a gold standard test for diagnosis of EIB in the literature. EVH has been shown to be superior in diagnosing EIB compared with methacholine or traditional exercise challenges (7,23). This difference likely is related to the fact that EVH allows a sustained and high level of minute ventilation when compared with treadmill challenges that may not produce minute ventilations sufficient to induce EIB in some athletes (9). The variable sensitivity of bronchoprovocation tests is an important consideration when comparing prevalence data from different studies.
In addition to the lack of a gold standard test, there is also a lack of consensus on the interpretation of many of the tests, including EVH. Proposed criteria for a positive EVH test include declines in FEV1 between 7 and 20% (5,8) or declines in any one or a combination of PEFR, FEV1, and forced expiratory flow between 25 and 75% of FVC (FEF 25-75) (14,16,22). The use of these various markers has obvious implications on prevalence rates. In our study, we report of prevalence of 39%, using declines in FEV1, FVC, or PEFR as criteria for EIB. Sixteen of 42 EIB-positive athletes (38%) were EIB positive by multiple criteria. However, if we had chosen to use a decline in FEV1 as our only criterion, our prevalence would be reduced to 19%, which is still elevated compared with normals but is significantly different than 39%.
In the only known published data evaluating the best parameters and thresholds for diagnosis of EIB using EVH testing, Hurwitz et al. (11) found that a decline of 10% of FEV1, 5% of FVC, or 20% of PEFR from baseline were all outside the range of a normal response and essentially equivalent criteria for a "positive" EVH test. In that study of 90 mild asthmatic and 30 nonasthmatics, receiver operator characteristic (ROC) curves were used to compare the accuracy of FEV1, FVC, FEF 25-75, and PEFR in predicting a diagnosis of EIB. Results show that FEV1 was more accurate than FEF 25-75 (P = 0.018) but was equivalent to FVC and PEFR (P = 0.4). Furthermore, data show that using declines of 10% of FEV1, 5% of FVC, or 20% of PEFR as diagnostics for EIB had specificities of greater than or equal to 90% for all three criteria and sensitivities of 66.3% for FEV1, 66.7% for FVC, and 66.7% for PEFR.
In another study, Mannix et al. (13) studied 124 figure skaters and found that EIB-negative athletes had no significant change in baseline FEV1 or FVC at any time point after exercise, but EIB-positive athletes had significant changes in both parameters after exercise. The study concluded that evaluating both FEV1 and FVC responses to exercise affords the greatest opportunity to diagnose EIB. Without a true gold standard test, however, there remains a lack of consensus about which EVH criteria are most predictive of EIB. Until more data are available, we would support the use of any one of the parameters found to be equivalent by Hurwitz et al. (11): decline of 10% of FEV1, 5% of FVC, or 20% of PEFR.
Our study is limited by a cross-sectional design and nonrandom evaluation of athletes from various sports, so the true prevalence in individual sports is unknown. In addition, although we did not find differences in the prevalence of EIB between males and females, our sample size for females was relatively small, especially in high-ventilation sports. Studies with larger numbers of athletes are needed to further investigate the prevalence of EIB in individual sports and how sex of the athlete affects EIB.
We found a 39% prevalence of EVH-defined EIB in a cohort of varsity college athletes. A large majority of EIB-positive athletes did not have a known prior history of EIB or asthma. There were not significant differences in prevalence according to the ventilation demands of the sport or the sex of the athlete. Reports of respiratory symptoms during exercise were not different between males and females and were not predictive of EIB. This raises important questions about the validity of a diagnosis of EIB that is based on subjective symptoms alone. Our results imply that empirically diagnosing and treating patients for EIB without objective testing likely will lead to inaccurate diagnoses and may lead to unnecessary morbidity. Future studies of athletes with EIB are needed to investigate the clinical significance of EIB and to guide recommendations on which athletes should be screened for EIB with objective tests before participation.
Funding for this study was provided by The Chest Foundation, National Center for Research Resources, K23 RR017579.
Dr. Parsons is a member of the Speakers' Bureaus of GlaxoSmithKline, Inc. and Schering-Plough, Inc. Dr. Mastronarde is a member of the Speakers' Bureaus of GlaxoSmithKline, Inc., Schering-Plough, Inc., and AstraZeneca, Inc.
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