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CLINICAL SCIENCES: Clinical Investigations

Bronchial Hyperresponsiveness in Skiers

Field Test versus Methacholine Provocation?


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Medicine & Science in Sports & Exercise: October 2007 - Volume 39 - Issue 10 - p 1681-1686
doi: 10.1249/mss.0b013e31813738ac
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Asthma represents an increasing problem for athletes competing within endurance sports. The prevalence of exercise-induced asthma (EIA) has increased during the last two decades, especially amongst elite endurance athletes (10,11,17). Heir and coworkers show that in competitive cross-country skiers, the prevalence of doctor-diagnosed asthma increased markedly up to 24% in the age group above 28 yr, in contrast to normally physically active control subjects (17). Larsson et al. (16) have demonstrated an alarmingly high prevalence of asthma and bronchial hyperresponsiveness (BHR) to methacholine in Swedish top-level cross-country skiers. Whereas BHR to methacholine has been regarded as a direct measure of nonspecific BHR, exercise-induced bronchoconstriction (EIB) and eucapnic hyperventilation test are looked on as indirect measures of nonspecific bronchial responsiveness (22). Weiler et al. (29) report a prevalence of EIA of 11% among American athletes participating in the 1984 summer Olympic Games, increasing to more than 20% among the American participants in the 1996 summer Olympic games in Atlanta, GA (28). As stated by Helenius et al., asthma occurs most commonly in athletes engaged in endurance sports such as cross-country skiing, swimming, or long-distance running. This is particular so for skiers (16), possibly because of the cold and dry air exposure during heavy exercise (19). In addition to the type of training, a major risk factor is atopic disposition (1,11).

The use of inhaled β2-agonists in asthmatic athletes at the Olympic games increased from 1984 and to later Olympic games (20). Reports and observations of frequent use of inhaled β2-agonists among top athletes led the IOC Medical Commission to make restrictions regarding the use of inhaled β2-agonists. From the Salt Lake City Olympic games, specific requirements were worked out, such as assessment of bronchial responsiveness, EIB, or reversibility to inhaled β2-agonists. These rules have later been modified. The present-day athletes must provide evidence of one of the following to be allowed to use inhaled β2-agonists (IBAs):

  1. a 12% or greater increase of the predicted or baseline value of FEV1 after administration of permitted IBAs;
  2. a 10% or greater decrease in FEV1 after challenge with physical stimuli, such as an exercise field test, exercise treadmill test in a laboratory, or eucapnic voluntary hyperventilation test (EVH); and
  3. obtaining by methacholine bronchial provocation test a dose of inhaled methacholine causing a reduction in FEV1 of 20% (PD20 methacholine) less than 2 μmol (400 μg) or a PC20 methacholine (concentration of methacholine) less than 4 mg·mL−1; for those on topical steroids, the methacholine PD20 has to be less than 13.2 μmol or the PC20 less than 13.2 mg·mL−1.

In this way, the IOC medical commission includes several tests for assessment of direct or indirect bronchial responsiveness for the athlete who wants to use inhaled β2-agonists in sports. Thus, how these tests compare in sensitivity and specificity for detecting BHR or EIB in the athlete with suspected asthma has impact on applications for and use of inhaled β2-agonists in international sport competitions.

Rundell et al. (24) report that by using real-life competitive events as the provoking agent among American participants in winter Olympic games, 98% of the athletes reporting EIA had positive tests. Also, 48% of the athletes not reporting EIA were found to have positive tests. They conclude that without relevant provoking agents, such as a sport-specific exercise field test (SSEFT), one might risk several false-negative results on screening for EIB or BHR among athletes (24). Ogston and Butcher (21) agree with Rundell et al., concluding that by using a sport-specific protocol, a large number of athletes can be screened objectively for EIB. On the other hand, Dickinson et al. (7) report that an EVH test is a more sensitive challenge in asymptomatic athletes than a sport-specific and laboratory-based challenge. Thus, this controversy is still unsolved. Therefore, the primary objective of the present study was to determine how a SSEFT compares in sensitivity with PD20 methacholine, in the assessment of asthma and BHR in elite cross-country skiers.


Design of the study.

The present study was an open study, nonrandomized, comparing indirect bronchial responsiveness as obtained by an exercise field test over a total of 7 and 10 km (♀ and ♂, respectively) with direct bronchial responsiveness obtained by a bronchial provocation test with methacholine measuring PD20 methacholine. The present study comprised 2 d.

  • Day 1: All subjects underwent a methacholine provocation test.
  • Day 2: All subjects competed in a cross-country skiing competition.

Before the provocation challenges, all athletes refrained from taking any medication that might have confounded the pulmonary function results. Antiasthmatic medications were withheld according to ERS guidelines (8). Inhaled, short-acting β2-agonists and sodium cromoglycate were withheld for 8 h before testing; inhaled, long-acting β2-agonists, theophylline, and leukotriene antagonists were withheld for the last 72 h; antihistaminics were withheld for the last 7 d; and orally administered glucocorticosteroids were withheld for the last month.

The study was performed according to the principles stated in the Declaration of Helsinki. The regional medical ethics committee approved the study, and all subjects gave written informed consent.


Twenty-four cross-country skiers, all competing at an international top level, participated in the study. All were members of the Norwegian national cross-country skiing team, five in the men's elite all-round team, eight in the women's elite team, six in the men's elite sprint team, and five male skiers in the recruit team. Demographics and baseline lung function (FEV1 and FEV1 % predicted) before the exercise field test are given in Table 1. Asthma treatment used before the study is reported in Table 2. The study took place at an altitude of 1100 m above sea level (masl) in the women's competition with a temperature of −2°C and a relative humidity of 36%, and at an altitude of 1250 masl during the men's competition with a temperature of −4°C and a relative humidity of 34%. Exclusion criteria were any acute or chronic illnesses interfering with the possibility to perform the study, in addition to upper-respiratory tract infections (URTI) during the 4 wk before testing.

Demographic data and baseline lung function (FEV1 and FEV1 percent predicted) before the exercise field test of the 24 elite skiers.
Gender, age, results of lung function measurements, exercise-induced bronchoconstriction (EIB), assessment of bronchial responsiveness to methacholine if the patients were diagnosed with asthma or atopy before the study, and treatment before and after the tests.

Lung function measurements.

Lung function was measured by maximum expiratory flow-volume loops according to the European Respiratory Society criteria (23); the best of three trials were recorded by use of Masterscreen Pneumo Jaeger (Würzburg, Germany). The following variables were recorded: forced vital capacity (FVC), forced expiratory volume in 1 s (FEV1), forced expiratory flow at 50% of vital capacity (FEF50), and peak expiratory flow rate (PEF).

Nonspecific bronchial responsiveness.

Nonspecific BHR was measured by bronchial provocation to methacholine. Methacholine was delivered by the inspiration triggered nebulizer Aerosol Provocation System Jäger (Würzburg, Germany) and was inhaled in doubling doses until FEV1 decreased 20% from baseline, as measured after inhaled nebulized isotonic saline. The dose causing a 20% reduction in FEV1 (PD20) was determined by linear interpolation on the semilogarithmic dose-response curve. All tests were performed according to current guidelines from the American Thoracic Society (4). After bronchial provocation testing, subjects were given salbutamol inhalations to reverse bronchial obstruction. BHR was defined as PD20 methacholine below 8 μmol.

Exercise challenge.

Lung function was measured before and after the exercise field test. The field test consisted of a cross-country skiing competition. The men performed a 10-km cross-country skiing competition, and the women performed a 7-km competition. The ambient temperature and the relative humidity during the cross-country skiing competition was measured and recorded. Lung function was measured by maximum expiratory flow-volume loops, as described above, before the start of the competition, immediately after finishing, and 5, 10, and 20 min thereafter. The term EIA has been used to denote symptoms and signs of asthma provoked by physical exercise, whereas EIB has been used to denote the measured decrease in lung function after an exercise test, as defined jointly by the Task Force on Sports and Asthma of the European Respiratory Society and the European Academy of Allergy and Clinical Immunology (2).

Statistical methods.

The present study included the entire Norwegian National team of cross-country skiers, 24 skiers altogether. Hofstra et al. (13) have reported previously that a sample size of 12 subjects is sufficient to assess differences in EIB. It was, therefore, concluded that a sample of 24 skiers was large enough to assess differences in the number of skiers positive to methacholine provocation compared with the number of skiers with positive exercise field tests.

Statistical analyses were performed with Statistical Package of Social Sciences version 11.0. Results are given as means with 95% confidence intervals unless otherwise stated. Demographics are given as mean with standard deviation in parentheses. Differences in categorical data were assessed by the Fisher exact test. Possible associations were assessed by the parametric Pearson's correlation coefficient. P values ≤ 0.05 (5%) was considered statistically significant.


Demographic variables of the cross-country skiers are shown in Table 1. PD20 methacholine < 16 μmol was found in 13 of 24 skiers (54.2%), in 3 of 8 females, and in 10 of 16 males, whereas 9 skiers (37.5%) had PD20 methacholine measurements below 8 μmol. The distribution of bronchial responsiveness to methacholine is shown in Figure 1. Two of 24 subjects (8.3%) experienced positive exercise field tests, a maximum reduction in FEV1 ≥ 10% (Table 2). Both had maximal reductions in FEV1 at 20 min after exercise. One of the skiers with a positive exercise field test had a positive methacholine provocation, with a PD20 methacholine of 5.79 μmol, whereas the other had a PD20 methacholine of 9.55 μmol (Table 2).

Inhaled dose of methacholine causing a 20% reduction in FEV1 (forced expiratory flow in 1 s compared with the number of skiers within each group (N = 24).

Subjects older than 25 yr (N = 9) of age had PD20 methacholine measurements below 8 μmol significantly more often than did subjects 25 yr and younger (N = 15; P = 0.036). One subject older than 25 yr was atopic, and three of the subjects ≤ 25 yr were atopic. All atopic subjects had PD20 values of 9.23 and below, and two were below 8 μmol. A significant negative correlation was found between age and log values of PD20 methacholine (r = −0.47, P = 0.02; Fig. 2). No significant difference in BHR to methacholine was found related to gender.

Scatterplot of lg PD20 methacholine vs age; regression line with 95% confidence interval. The lg PD20 methacholine values of 0.3, 0.6, 0.9, and 1.20 are equivalent to 2.0, 4.0, 8.0, and 16.0 μmol of methacholine, respectively. ♂ male; ♀ female (r = −0.47, P = 0.02). N= 24; 9 subjects were older than 25 yr, and 15 subjects were 25 yr or younger.


The present study suggests that PD20 methacholine is more sensitive than exercise field testing using the competitive sport to assess BHR in elite cross-country skiers. Nine athletes experienced PD20 < 8 μmol (37.5%), and 13 (54.2%) were less than 16 μmol. On the contrary, only two subjects experienced positive exercise field tests and maximum reductions in FEV1 ≥ 10%. One of the two did not use any medication (Table 2). A significantly higher percentage of BHR among subjects older than 25 yr compared with younger subjects was found (Fig. 2).

The present study supports the findings of Dickinson et al. (7), concluding that a sport-specific exercise test is not the best challenge for diagnosing EIB or BHR. They suggest that an EVH test provides a more sensitive diagnosis of BHR in elite winter athletes. In accordance with Dickinson et al. (7), our findings do not agree with the findings of Rundell et al. or those of Ogston and Butcher, suggesting that a sport-specific exercise field test is the method of choice in the diagnosis of EIB among top athletes (21,24). Exercise field tests were recommended for the Olympic games in Salt Lake City in 2002 because they were considered effective and more sensitive for identification of EIB in cold-weather athletes when compared with exercise performed under laboratory conditions of temperature and humidity (18,30). It can be assumed that by performing one's usual exercise in the usual environment, the athlete would be in the best position to reproduce his or her respiratory problems. However, in the present study, the sport-specific exercise field test did not reveal any subjects who had not already been recognized by the PD20 methacholine test, and 11 of 13 subjects with some degree of BHR to methacholine were not detected by the exercise field test (24).

Crimi et al. (5) claim that direct stimuli such as methacholine can allow the identification of asthmatic subjects who do not exhibit EIB because of a low degree of airway inflammation at the time of study but who may eventually become ill if exposed to sensitizing allergens or after virus infections. Langdeau et al. (15) investigated the Canadian Olympic team and found that nearly 50% were positive to methacholine compared with 18% of healthy controls. This is in concordance with the findings of the present study.

A significantly higher percentage of BHR was found among subjects older than 25 yr of age (P = 0.036). This agrees with the findings of Heir et al., who have demonstrated by their questionnaire study a higher prevalence of doctor-diagnosed asthma among cross-country skiers with increasing age compared with healthy control subjects (10). One possible explanation may be that the continued stress to the airways over many years caused by high ventilation rates during exercise, often in dry, cold environments, increases BHR over time by increasing airway inflammation. This was also found by Sue-Chu et al. (25) and Karjalainen et al. (14) in their bronchial biopsy study of young skiers from a skiing high school. This was also confirmed in a study on exercising mice with increasing epithelial damage with continued exercise (3). Others speculate that immune suppression may contribute in the development of BHR, at least in endurance athletes (6,9,26). Heir et al. (9) found that training with an URTI induced a long-lasting (≥ 6 wk) increase in BHR to histamine, whereas this did not occur in subjects who did not train actively during the infection.

No significant gender difference was found in the present study with 6 of 16 men, and 3 of 8 women displayed BHR to methacholine with PD20 values below 8 μmol. Former studies have implied a slightly higher prevalence in female athletes (16,30), and women have been shown to have a slightly higher prevalence of BHR to methacholine (12,27). The number of athletes participating in the present study may have been too low to assess significant differences to gender.

The present study fully demonstrates the discrepancy between direct and indirect tests of bronchial hyperresponsiveness. Furthermore, it should be emphasized that asthma is a clinical diagnosis based on reports of recurring episodes of bronchial obstruction. Both direct and indirect BHR change over time because of changing exposure to allergens and other environmental agents, as well as being dependent on antiinflammatory treatment. The diagnosis of asthma in athletes should be based on a combination of clinical history and clinical signs with the use of supplementary objective tests as used in the present study. For practical purposes, this is important also in relation to the rules given by the IOC medical commission and the World Anti-Doping Association for the use of asthma drugs in sports.

In conclusion, the present study demonstrates that measurement of BHR to methacholine is more sensitive than exercise field testing in confirming the diagnosis of BHR or EIB in elite cross-country skiers.


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