Background There is increasing evidence to suggest many elite athletes fail to recognise and report symptoms of exercise-induced bronchoconstriction (EIB), supporting the contention that athletes should be screened routinely for EIB.
Purpose To screen elite British athletes for EIB using eucapnic voluntary hyperpnoea (EVH).
Methods 228 elite athletes provided written informed consent and completed an EVH challenge with maximal flow volume loops measured at baseline and 3, 5, 10 and 15 min following EVH. A fall of 10% in forced expiratory volume in 1 s (FEV1) from baseline was deemed positive. Two-way analysis of variance was conducted to compare FEV1 at baseline and maximal change following EVH between EVH-positive and EVH-negative athletes who did and did not report a previous diagnosis of EIB. Significance was assumed if p≤0.05.
Results Following the EVH challenge 78 athletes (34%) demonstrated EVH positive. 57 out of the 78 (73%) athletes who demonstrated EVH positive did not have a previous diagnosis of EIB. 30 athletes reported a previous diagnosis of asthma, nine (30%) of whom demonstrated EVH negative. There was no significant difference between the magnitude of the fall in FEV1 between athletes who reported a previous diagnosis of EIB and demonstrated EVH positive, and those with no previous diagnosis of EIB who demonstrated EVH positive (mean±SD; −21.6±16.1% vs −17.1±9.7%; p=0.07).
Conclusion The high proportion of previously undiagnosed athletes who demonstrated EVH positive suggests that elite athletes should be screened routinely for EIB using a suitable bronchoprovocation challenge.
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Exercise-induced bronchoconstriction (EIB) is closely related to asthma and is defined as a transient narrowing of the airways, limiting expiration that usually follows a bout of exercise, and is reversible spontaneously or through the inhalation of β2 agonists.1 Our group has previously reported the prevalence of EIB in British olympic athletes to be approximately 20%,2 which is higher than the prevalence of asthma in the general population (∼8% in UK adults).3 In sports such as swimming and cycling EIB prevalence has been reported to range between 39% and 44%.2 The high prevalence of EIB in these types of sports is thought to be due to the training/competition environment and ventilatory requirements.
The eucapnic voluntary hyperpnoea (EVH) challenge is a surrogate for exercise,4 and has been demonstrated to possess a high specificity and sensitivity in the diagnosis of EIB in elite athletes.5 Therefore, the International Olympic Committee Medical Commission (IOC–MC) recommends that athletes are tested for EIB using EVH challenges in order to provide evidence of EIB and use inhaled β2 agonists while competing at Olympic games.6
Studies that have used objective tests, such as EVH, have identified an alarming subgroup of athletes, who have no previous diagnosis of EIB, but who exhibit a positive response to EVH.2 5 7,–,9 This has led to the suggestion that elite athletes should be screened periodically for EIB using bronchoprovocation challenges, irrespective of symptoms and previous diagnosis.10 The purpose of this study was thus to screen 228 elite British athletes from a range of sports for EIB using an EVH challenge. The sample included apparently healthy individuals, and those with a previous diagnosis of EIB, but without a previous bronchoprovocation challenge.
Following ethical approval from Harrow Local Research Ethics Committee, England, the medical teams of rugby union, British international rowing, England hockey, England women's football, England badminton, UK athletics, British biathlon and British short track speed skating were approached to give consent to screen their national squads using an EVH challenge. Two hundred and twenty-eight elite athletes (mean±SD age 24.0±4.1 years, stature 182.0±9.6 cm, body mass 86.3±17.8 kg) were invited for testing and all 228 volunteered and provided written informed consent. To our knowledge, none of the athletes had completed a previous bronchodilator or bronchoprovocation challenge. The EVH challenges took place between February 2006 and January 2007, between 08:00 and 18:00 hours.
Each athlete was required to state whether they had a previous diagnosis of EIB and what breathing symptoms they experienced during and following exercise. Athletes indicated whether they experienced coughing, chest tightness, difficulty in breathing (dyspnoea) or excess mucus production. No other symptoms were queried. Athletes were also asked whether exposure to an environment high in pollen increased the severity of their symptoms.
Athletes using asthma medication were instructed to cease using their medication before the EVH challenge (inhaled corticosteroids: 3 days before; inhaled long-acting β2 agonists: 2 days before; inhaled short-acting β2 agonists: the day of the test). Athletes were asked to avoid aerobic exercise and caffeine consumption on the test day. Athletes were tested at least 2 weeks after any chest or upper respiratory tract infections.
Baseline forced expiratory volume in 1 s (FEV1) was recorded from the best of three maximal voluntary flow-volume loops. All athletes had a baseline value greater than 70% of their predicted value (baseline FEV1 predicted value range 78–134%).11 Therefore the EVH challenge could be carried out on all athletes. The EVH challenge required athletes to achieve a target minute ventilation (V·E) of 85% (baseline FEV1 × 30) of their predicted maximal voluntary ventilation rate (MVV) for 6 min.4 The air that was inspired during the EVH challenge consisted of 21% oxygen, 5% carbon dioxide and 74% nitrogen (inspired air temperature 19°C, humidity <2%). The gas was delivered to each participant by means of a gas cylinder, reservoir and a two-way valve. V·E was recorded by calculating the volume of air passing through a dry gas meter every minute. After stopping the EVH challenge maximal voluntary flow-volume loops were measured at 3, 5, 10 and 15 min. Two flow-volume loops were collected at each time point. The maximal flow-volume loop with the highest FEV1 was recorded at each time point. A test was deemed positive for EIB if the FEV1 fell by at least 10% from baseline at two consecutive time points following EVH.6 If the athlete's FEV1 was less than 10% of their baseline after the challenge they were offered 200 µg inhaled β2 agonist. Athletes were asked to remain in the laboratory until their FEV1 was within 10% of their baseline measurement.
A MicroLab ML3500 (Cardinal Health, Basingstoke, UK) spirometer was used to collect all spirometry measurements. FEV1, peak expiratory flow (PEF), forced vital capacity (FVC), forced expiratory flow at 50% of FVC (FEF50) and the FEV1:FVC ratio (FEV1/FVC) were recorded at each time point. Individual maximal flow-volume loops were accepted in accordance with European Respiratory Society/American Thoracic Society criteria.12
Athletes were grouped according to whether they demonstrated a positive or negative EVH challenge, and according to whether they reported having a previous diagnosis of EIB. One-way analysis of variance (ANOVA) was conducted to compare baseline FEV1, PEF, FVC, FEF50 and FEV1% between EVH-positive and EVH-negative athletes, with and without a previous diagnosis of EIB. Mixed model repeated measures ANOVA compared FEV1 at rest and at 3, 5, 10 and 15 min post-EVH challenge between EVH-positive and EVH-negative athletes. If a significant interaction was demonstrated, one-way ANOVA was used to compare means at each time point between groups and repeated measures ANOVA was used to compare means at pre, 3, 5, 10 and 15 min within each group. Two-way ANOVA was also used to evaluate EVH response, previous EIB diagnosis, reported symptoms and their interaction. χ2 Analysis was used to evaluate the reported symptoms between EVH-negative and EVH-positive athletes with and without a previous diagnosis of EIB. A p value of 0.05 or less was deemed significant in all analyses. Unless otherwise stated, all data are reported as mean±SD. All analysis were conducted on the statistical software package SPSS 17.0.
All 228 athletes were able to complete the EVH challenge. Table 1 summarises the results of the EVH challenge. There were 30 (13%) athletes with a previous EIB diagnosis. They reported using one or a combination of short-acting inhaled β2 agonists, long-acting inhaled β2 agonists and inhaled corticosteroids (table 2).
EVH-positive athletes with a previous diagnosis of EIB had a significantly (p<0.01) lower predicted value of FEV1 when compared with EVH-negative athletes with no previous diagnosis of EIB. Actual and predicted values for FEV1/FVC and FEF50 were significantly lower in EVH-positive athletes regardless of the previous diagnosis when compared with EVH-negative athletes with no previous EIB diagnosis (table 3).
The mean maximum change in FEV1 was −18.3±11.9% (range −10% to –68%) in EVH-positive athletes, which was a significantly (p<0.01) greater change when compared with the mean maximum change in FEV1 of −4.6±2.9% (range 5% to −9%) in EVH-negative athletes (figure 1). Mixed model repeated measures ANOVA demonstrated a significant interaction between EVH-positive and EVH-negative athletes and the FEV1 measurements taken at 3, 5, 10 and 15 min post-EVH challenge (p<0.01) (see figure 2). FEV1 was significantly lower at each time point following the EVH challenge in EVH-positive athletes when compared with EVH-negative athletes (p<0.01). Within EVH-positive athletes the FEV1 measurement taken at 5 min (−16.7±12.0%) was significantly lower than the FEV1 measurements at 3 (−14.9±10.7%; p=0.01), 10 (−13.4±8.3%; p<0.01) and 15 (−10.2±4.5%; p<0.01) min, respectively. χ2 Analysis demonstrated that it was the 5 min measurement in which the lowest FEV1 value was recorded most frequently (p<0.01). There was no significant difference in the percentage of MVV reached during the EVH challenge between EVH-positive and EVH-negative athletes (79.1±11.2% vs 79.5±9.8%; p=0.77). The percentage of MVV achieved during the EVH challenge ranged from 50% to 118%. During the EVH challenge eight athletes achieved less than 60% of predicted MVV, of which two presented EVH positive (figure 1). The magnitude of the fall in FEV1 was the same in EVH-positive athletes who had a previous diagnosis of EIB and EVH-positive athletes who had no previous diagnosis of EIB (−21.6±16.1% vs −17.1±9.7%; p=0.07). There were significant differences in the maximum changes in FVC (−6.2±8.3% vs −1.5±3.2%; p<0.01), PEF (−18.0±12.5% vs −6.4±5.9%; p<0.01), FEF50 (−34.0±15.8% vs −10.2±12.2%; p<0.01) and FEV1/FVC (−13.2±7.7% vs −3.3±3.1%; p<0.01) following the EVH challenge between EVH-positive and EVH-negative athletes.
The symptoms reported by athletes are presented in table 4. χ2 Analysis revealed that cough was the most reported symptom regardless of the EVH result and history of EIB (p<0.01). The symptoms of wheezing (p<0.01), tight chest (p<0.01), dyspnoea (p<0.01) and excess mucus production (p<0.02) were reported with significantly more frequency in athletes with a previous history of EIB when compared with those with no previous history. There was no difference (p>0.05) in the frequency of reports of wheezing, tight chest, dyspnoea and excess mucus production between EVH-positive and EVH-negative athletes with a previous history of EIB.
Forty-two athletes (18 EVH negative; 24 EVH positive) reported a worsening of respiratory symptoms when exposed to a high pollen environment. EVH-positive athletes who reported increased respiratory symptoms in environments high in pollen had a significantly (p<0.01) greater change in FEV1 following EVH (−24.2±17.9%) when compared with EVH-positive athletes who did not report any increased respiratory symptoms in a pollen environment (−15.7±6.87%). EVH-negative athletes did not show any difference between those who indicated that high pollen environments made respiratory symptoms worse and those who did not (−5.1±2.7% vs −4.5±2.9%; p=0.37).
This is the first study to screen a large number of elite British athletes using an EVH challenge. We found that following the EVH challenge 78 out of 228 (34%) athletes demonstrated EVH positive. The number of athletes that demonstrated EVH positive was similar to other reports that have used EVH to screen a sub-elite population of athletes,9 and those that have used exercise challenges to screen an elite population of athletes.13
The IOC–MC requires every request to use inhaled β2 agonists to be accompanied by evidence of bronchoconstriction through a bronchodilator or bronchoprovocation challenge.6 The progressive increase in the number of athletes requesting to use inhaled β2 agonists at previous Olympic games was one of the reasons cited for the IOC–MC's ruling. It is reasonable to assume that, after the introduction of their objective criteria, the IOC–MC anticipated a reduction in the number of athletes requesting the use of inhaled β2 agonists. Similarly, it is reasonable to assume that the IOC–MC believed that many athletes were using inhaled β2 agonists unnecessarily. Contrary to this hypothesis, data from our group suggested that the prevalence of EIB within team GB remained unchanged between the summer games of 2000 and 2004.2 Although other countries did observe a reduction in the number of requests to use inhaled β2 agonists in their 2004 Olympic teams due to this change in criteria.14 However, importantly, our previous study2 highlighted a surprising phenomenon, ie, a proportion of elite competitors were unaware that they had EIB. In our present study 57 (73%) of the 78 EVH-positive athletes had no previous diagnosis of EIB. This confirms our previous observations that a high proportion of elite British athletes are currently competing with uncontrolled EIB. The problem of EIB within British elite sport thus appears to be one of underdetection, rather than of over-diagnosis and abuse of inhaled β2 agonists. This study indicates that rigorous screening of elite athletes for EIB using the EVH challenge will identify a significant number of EVH-positive athletes, with no previous EIB diagnosis, who may benefit from appropriate pharmacological treatment strategies.
A recent review concluded that inhaled β2 agonists have no ergogenic effect and questioned the continued inclusion of inhaled β2 agonists on the list of prohibited substances.15 However, there has been an unforeseen benefit of this inclusion, and the associated burden of proof for the use of inhaled β2 agonists in competition, that is, that the number of athletes who are subjected to bronchoprovocation challenges has increased. Our data suggest that this seemingly onerous and meaningless requirement will in fact make a very positive impact upon athlete care, because it appears that a significant proportion of athletes are not currently receiving adequate management of their EIB. Indeed, out of the group with no previous diagnosis of EIB who presented with a positive EVH challenge there were five who had a maximal fall in FEV1 from their baseline measure of 30% or more, the greatest being a 60% fall. It is paramount that all athletes with EIB are detected as acute cases of bronchoconstriction can result in significant mortality.16
The risk of acute bronchoconstriction in elite athletes can be reduced through the early detection of EIB and suitable treatment.17 In particular, the regular use of inhaled corticosteroids has been shown to provide significant prevention against airway inflammation and bronchoconstriction, even in those with mild airway hyperresponsiveness.18,–,20 In the present study, 14 out of the 30 athletes previously diagnosed for EIB were managing the disease solely through the use of a short-acting β2 agonist. Caution must be taken if athletes are treated solely through short or long-acting β2 agonists, as potential side-effects have been noted.21 Following the EVH screening all EVH-positive athletes were prescribed a minimum of inhaled corticosteroid and a short-acting β2 agonist.
In the present study, nine athletes demonstrated EVH negative, despite a previous diagnosis of EIB. In this study we did not conduct further bronchoprovocation testing nor did we thoroughly investigate atopy in the athletes. It must be understood a characteristic of EIB is that it has a high degree of variability. Athletes can demonstrate EVH negative, but still experience EIB for a number of reasons, including being well-controlled with inhaled corticosteroids, being in a period of remission or the EIB being linked to specific allergens such as pollution or pollen. Furthermore, some studies have suggested that the cut-off criterion used to diagnose EIB following recognised bronchoprovocation is not suitable for elite athletes and may result in athletes with EIB being denied the most effective therapeutic treatment(s).22,–,24 Therefore, an athlete who is EVH negative, but has either symptoms and/or a previous diagnosis of EIB, should not immediately be deemed EIB negative. Indeed, it is recommended that all those who are EVH negative but have a previous history of EIB and/or are significantly symptomatic, should be advised to undertake further testing, such as a mannitol challenge or sports-specific exercise challenge. In addition, athletes who cannot provide evidence of reversible bronchoconstriction can still submit a detailed history of their EIB condition including hospital admissions to the IOC–MC in order to obtain a therapeutic use exemption certificate to inhaled β2 agonists in Olympic competition.6 A balance should thus be sought between the results of appropriate airway challenge testing, and information regarding an athlete's medical history, in order to make the appropriate diagnosis of EIB and to provide optimal therapeutic care to the athlete.
It is not uncommon for athletes with inspiratory stridor to be misdiagnosed with EIB.13 To the investigators' knowledge, two of the EVH-negative athletes with a history of EIB who presented with a negative EVH challenge were found subsequently to have inspiratory stridor and dysfunctional breathing during high-intensity exercise. There are non-pharmacological treatment strategies that can be used to assist these athletes who would otherwise be prescribed inhaled β2 agonists to no benefit.25
Of the 78 athletes who demonstrated EVH positive, only 46 (59%) reported at least one symptom of EIB. Our data therefore confirm indications from previous studies regarding the fallibility of symptoms.26 27 A recent study by Lund et al26 demonstrated that out of 42 symptomatic elite athletes, only 12 could provide objective evidence of asthma. Rundell et al27 showed that only 50% of athletes who had genuine EIB reported any symptoms of EIB. This would suggest that many elite athletes fail to associate respiratory symptoms with EIB, perhaps believing their extreme dyspnoea to be a normal part of intense training/competition. In addition, some athletes may believe that reporting symptoms of EIB shows weakness, and they fear that their place on the team/squad may be at risk. Therefore, if routine screening programmes are implemented, both athletes and coaches must be reassured that athletes with EIB can be well managed with appropriate medication, and are at no disadvantage compared with their non-EIB counterparts.17
It is relevant to acknowledge that the high prevalence of EIB observed in our sample may have been biased by the fact that we predominantly tested athletes from sports with high ventilatory requirements (ie, rugby, rowing, hockey, athletics, football, biathlon and speed skating). These sports are thought to be more ‘asthmogenic’ as athletes inhale large volumes of ‘unconditioned’ air though their mouth into the lower airways, which may result in an airway remodelling and the development of airway responsiveness.28,–,30
We must acknowledge that the EVH challenge is a highly sensitive challenge and is a surrogate for exercise to diagnose athletes with EIB. The V·E (∼85% of MVV) and dry air (<2% humidity) that underpin the EVH challenge are not entirely representative of the ventilatory requirements and environment of most sports. Therefore the EVH challenge is a relatively aggressive challenge when compared with a sports-specific exercise challenge. Therefore any reduction in FEV1 observed following an EVH challenge may be less pronounced during the athletes' training or competition. However, if an athlete does demonstrate EVH positive the result suggests the athlete is at risk from EIB during or following exercise. An appropriate course of action in such situations is to establish appropriate treatment plans including pharmacotherapy. This minimises the risk of a life-threatening exacerbation, as well as ensuring that any mild EIB does not impair their performance.
What is already known on this topic
Exercise-induced bronchoconstriction has a high prevalence within elite sport. It can be detected through a variety of recognised bronchoprovocation challenges, and once confirmed the condition can be managed through appropriate pharmacotherapy treatments.
What this study adds
▶ A significant number of elite athletes who are competing do not recognise they have EIB.
▶ Screening elite squads using bronchoprovocation challenges, such as EVH, allows the detection of these athletes.
▶ The detection of previously unrecognised EIB may lead to improvements in athlete's health and performance.
Regardless of the position of inhaled β2 agonists on the list of prohibited substances, this study demonstrates that screening athletes for EIB results in the detection of athletes who may benefit from use of appropriate medication to treat EIB. The high proportion of asymptomatic athletes who demonstrated EVH positive suggests that all elite athletes should be screened routinely for EIB using a suitable bronchoprovocation challenge, such as EVH.
This paper is dedicated to the memory of Dr Mark Harries. The authors are grateful to the European Olympic Committee, UK Sport, British Olympic Medical Trust, Olympic Medical Institute, English Institute of Sport and Micro Medical (http://www.micromedical.co.uk).
Competing interests None.
Patient consent Obtained.
Ethics approval This study was conducted with the approval of the Harrow Local Research Ethics Committee, England.
Provenance and peer review Not commissioned; externally peer reviewed.
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