ABSTRACT
Background
Exercise‐induced bronchoconstriction (EIB) is common among adolescents and athletes. While typically assessed with spirometry, oscillometry may offer complementary insights. This cross‐sectional study examined how fractional exhaled nitric oxide (FeNO) and symptoms relate to postexercise airway responses assessed via spirometry and oscillometry, and whether these associations differ between nonathletes and athletes.
Methods
Subsamples from two adolescent cohorts (N = 241; 143 nonathletes, 98 athletes) completed questionnaires, FeNO measurements, and an EIB test using spirometry, by change in forced expiratory volume in 1 s (∆FEV1), and oscillometry, by change in resistance and reactance at 5 Hz (∆R5, ∆X5). Correlations were assessed using Spearman's rank; logistic regression evaluated associations between elevated FeNO and EIB; linear regression explored links between symptoms and postexercise airway responses.
Results
EIB was detected in 70 participants via spirometry (∆FEV1 ≤ −10%), 81 via oscillometry (∆R5 ≥ 25%), and 37 by both. Among nonathletes, FeNO was weakly correlated with ∆FEV1 (r s = −0.17, p = 0.04), ∆R5 (0.35, p < 0.001), and ∆X5 (−0.25, p = 0.005). Elevated FeNO (> 20 parts per billion) was associated with EIB by ∆FEV1 (aOR 2.54, 95% CI: 1.05–6.12) and ∆R5 (aOR 3.05, 95% CI: 1.18–7.9). Respiratory symptoms also related to postexercise airway responses in nonathletes. In contrast, no such associations were observed in athletes.
Conclusion
In nonathletes, elevated FeNO and symptoms can indicate who needs EIB testing. These indicators were less predictive in athletes, emphasizing the value of objective assessment. Oscillometry was complementary to spirometry to assess EIB and a combination of methods might be more informative.
Keywords: adolescents, athletes, bronchial challenge, exercise, exercise‐induced bronchoconstriction, forced oscillation technique, general population
1. Introduction
Experiencing airway symptoms, such as dyspnea or wheeze, in conjunction with exercise is common in adolescents [1] and is associated with negative health consequences [2]. Among adolescents and young adults participating in competitive sports, airway symptoms are more prevalent than among adolescents in the general population [3, 4]. Similar exercise‐induced airway symptoms can be present in various conditions, for example, exercise‐induced laryngeal obstruction (EILO) [5], or perhaps most commonly, exercise‐induced bronchoconstriction (EIB) [6]. Thus, standardized testing is recommended as part of the clinical assessment of adolescents with exercise‐induced airway symptoms [7].
Exercise‐induced bronchoconstriction (EIB) is a transient narrowing of the lower airways triggered by exercise [6]. In children and adolescents, EIB prevalence is higher than in the general adult population, ranging from 3% to 35% [8]. Among elite athletes, EIB is widely observed, yet reported prevalence varies substantially depending on the type of sport, athletic environment, and diagnostic method [9]. The diagnostic approach for EIB comprises evaluation of change in airway calibre after a standardized bronchial challenge, for example, an exercise test, eucapnic voluntary hyperpnea or inhaled hypertonic agents. The post‐challenge change in airway calibre is usually assessed by dynamic spirometry, where a change in forced expiratory volume in 1 s (FEV1) of ≤−10% is considered positive for EIB [10]. Several studies have reported poor agreement between self‐reported airway symptoms and having EIB objectively confirmed by a bronchial challenge. This discordance has been described in studies of adolescents from the general population [11, 12], but seems even more pronounced in athletes [4, 13], emphasizing the role of objective assessment of airway response to a standardized bronchial challenge.
Forced oscillations technique (FOT) is a method for measuring the mechanical properties of the respiratory system during tidal breathing. Oscillations are superimposed over the individual's spontaneous quiet breathing, assessing resistance and reactance of the airways [14]. Oscillometric indices can be valuable when diagnosing asthma in individuals with normal spirometry and are reported to be more sensitive to airway narrowing than spirometry [15]. The association between self‐reported airway symptoms and oscillometric measurements is reported to be stronger compared with spirometry in both patients with asthma [16] and in the general population [17]. Oscillometric parameters as measures of postexercise airway responses have been reported to be sensitive for the detection of bronchoconstriction in asthmatic children [18, 19] and in adults with asthma [20, 21]. Oscillometry in relation to postexercise airway responses has also been evaluated in population‐based groups, i.e. not clinically selected on asthma diagnosis, of adolescents [22] and in adult recreational athletes [23]. These studies report some discrepancies regarding EIB assessed by spirometry and oscillometry, as some individuals are EIB‐positive by one modality and not the other.
Fractional exhaled nitric oxide (FeNO) is a type‐2 airway inflammation biomarker [24]. FeNO has been associated with objectively confirmed EIB in asthmatic children [25] and in population‐based studies of children and adolescents [26, 27]. However, the usefulness of FeNO as a predictor of EIB in athletes remains uncertain [28].
We aimed to study the relationships between respiratory symptoms, FeNO and postexercise airway responses measured by spirometry and oscillometry in adolescents—one group sampled from the general population and one from students attending a sports high school. We hypothesize that associations between respiratory symptoms and FeNO and EIB differ between adolescents from the general population compared with high school athletes.
2. Methods
The study population (N = 241) comprised subsamples from two cohorts of adolescents, the ANDAS cohort sampled from the general population, and the CELADY cohort sampled from high school athletes. In these two cohorts previous studies have evaluated the prevalence of EIB [4, 12]. In both cohorts, the participants were invited to answer a questionnaire on respiratory symptoms, asthma and allergy. The randomly selected participants, stratified by self‐reported exercise‐induced dyspnea (EID), were invited to a clinical visit where a standardized exercise test to investigate EIB was performed. The ANDAS cohort enrolled 2309 adolescents (age 14.2 years) from the general population living in the Uppsala region, of whom 143 participants performed the EIB test with complete spirometry and oscillometry data. This cohort has previously been studied regarding oscillometry and EIB, but with another focus; analyzing changes in oscillometry after exercise in the same population, divided by the presence of EIB (ΔFEV1 ≤ −10%) and EID [22]. In the ANDAS cohort, it has previously been reported an association between elevated FeNO, using a different threshold than in the present study (> 20 parts per billion [ppb]), and EIB defined by spirometry, as well as an association between EID and EIB defined by spirometry [27]. The CELADY cohort enrolled 367 adolescent athletes (age 15.8 years) during their first year in sports high school, of whom 98 participants performed the EIB test with complete spirometry and oscillometry data. Following a selection process based on athletic performance within their respective disciplines—spanning 21 different sports—the students were admitted to the sports high school, rendering a selected population of high level student athletes, many of them pursuing a future elite career. In the ANDAS study, the sampling ratio EID: non‐EID was set to 2:1, while in CELADY, the ratio was set to 1:1. The cohorts will henceforth be defined as nonathletes (sampled from the general population) and athletes (sampled from sports high school).
2.1. Questionnaire
The questionnaire has previously been employed in adolescent cohorts [4, 12]
Occurrence of EID and wheeze was assessed by the following questions: “Have you in the last 12 months at one or more occasions had an attack of shortness of breath during or after exercise?” and “Have you at any time in the last 12 months had wheeze or whistling in your chest?”
Current asthma was defined as having a previous asthma diagnosis from a physician and experiencing respiratory symptoms in the past 12 months and/or having asthma treatment in the last 3 months.
2.1.1. Fractional Exhaled Nitric Oxide (FeNO)
All FeNO measurements were conducted during the clinical visit for the exercise‐induced bronchoconstriction (EIB) test, preceding oscillometry, spirometry, and exercise challenge.
FeNO was assessed twice at a flow rate of 50 mL/s (NIOX Vero; Circassia) following the technical guidelines outlined by the American Thoracic Society/European Respiratory Society [29]. Mean values are reported in the present paper.
2.1.2. Exercise‐Induced Bronchoconstriction Test
The participants were instructed to avoid vigorous physical activity, caffeine, nicotine, and heavy meals within 4 h before the test. They were also instructed to refrain from any short‐acting β2‐agonists 8 h before the test, long‐acting β2‐agonists 24 h before the test, leukotriene receptor agonists 72 h before the test and inhaled corticosteroids on the day of the test.
Baseline lung function measurements by FOT (Resmon Pro Full, Restech Srl) and spirometry (CardioPerfect dynamic spirometry; Welch Allyn) were performed before a treadmill exercise challenge. FOT, with a multifrequency signal of 5, 11 and 19 Hz, was measured in duplicates. Baseline respiratory resistance at 5 Hz (R5) and respiratory reactance at 5 Hz (X5) was calculated as the mean of two acceptable measurements, comprising 10 acceptable breaths. Spirometry was conducted in accordance with ATS/ERS guidelines [30], and FEV1 was documented as the highest of three acceptable and reproducible manoeuvres (the two highest values within 150 mL of each other). The participants exercised for 7–8 min while wearing a nose clip and breathing dry air through a tubing system connected to a central gas container (H2O < 5 mg/L, 18°C–22°C). Heart rate was monitored continuously, and the protocol required reaching 90% of the predicted maximum heart rate ((220—age) × 0.9) within the first 2 min and maintaining this level of exercise for 5–6 min. Postexercise FOT (single measurements with at least five artefact‐free breaths) and spirometry (duplicate measurements) were performed at 5, 10, 15, and 30 min after exercise cessation.
EIB was defined as a decline in FEV1 ≤ −10% from baseline at any time point postexercise [10]. Similarly, an increase in R5 ≥ 25% was used as the cutoff for a positive airway response measured with FOT [21]. Investigators K. E. and H. J., who supervised all the EIB tests, were blinded to the participants’ answers to the questionnaires.
2.2. Statistical Methods
Shapiro–Wilks's test assessed the normality of continuous variables. Continuous variables that followed a normal distribution were expressed as means with standard deviations (SD). In contrast, those with non‐normal distributions were presented as medians with interquartile ranges (Q1–Q3) or as geometric means with 95% confidence intervals (95% CI) (the last‐named only for FeNO that had a skewed distribution to the right). Postexercise airway responses were defined as ∆FEV1 as % change from baseline to nadir after exercise; ∆R5 as % change from baseline to peak after exercise; ∆X5 as the change in actual values from baseline to nadir after exercise. Correlations between log‐transformed FeNO and ∆FEV1, ∆R5 and ∆X5, respectively, were analyzed with Spearman's rank correlation coefficient. Logistic regression models were used to examine the associations between elevated FeNO defined as FeNO ≥ 25 ppb (as exposure) and EIB defined by ∆FEV1 ≤ −10% and ∆R5 ≥ 25% (as outcomes), yielding odds ratios (OR) and 95% CI. The logistic regression models were adjusted for height and sex. The relationships between wheeze and EID (as exposures) and ∆FEV1, ∆R5 and ∆X5 (as outcomes) were analyzed using linear regression models, yielding β‐coefficients and 95% CI. Statistical significance was considered at p < 0.05.
All analyses used STATA 15.1 (College Station, TX: Stata Corp LLC).
3. Results
The athletes competed in their sports disciplines at international, national, and regional levels. Within the group, 21 different sports disciplines were represented. Soccer, floorball, American football, basketball, and orienteering were the most common disciplines.
The baseline characteristics of the participants are presented in Table 1.
Table 1.
Baseline characteristics of the participants.
| Nonathletes (n = 143) | Athletes (n = 98) | |
|---|---|---|
| Female, n (%) | 86 (62.1) | 57 (58.2) |
| Age (years), median (Q1–Q3) | 14 (14–15) | 16 (15–16) |
| Height (cm), median (Q1–Q3) | 168 (163–175) | 172 (167–180) |
| BMI to age,a n (%) | ||
| Overweight > + 1 SD | 29 (20.2) | 24 (24.5) |
| Normal −2SD to +1 SD | 108 (75.5) | 73 (74.5) |
| Thinness < −2SD | 6 (4.2) | 1 (1) |
| Rhinitis, n (%) | 48 (33.6) | 26 (27.6) |
| Current asthma,b n (%) | 43 (30.1) | 21 (21.4) |
| Wheeze,c n (%) | 56 (39.2) | 34 (34.7) |
| Exercise‐induced dyspnea,c n (%) | 97 (67.8) | 41 (41.8) |
| ICS,d n (%) | 23 (16.1) | 11 (11.8) |
| FeNO (ppb), geometric mean (95% CI) | 14.5 (13.0, 16.2) | 16.2 (14.7, 17.9) |
| Elevated FeNO (≥25 ppb), n (%) | 26 (18.2) | 20 (20.4) |
| FEV1% predicted,e mean (SD) | 92.5 ( ± 10.2) | 95.8 ( ± 10) |
| Abnormal FEV1/FVC ratio,f n (%) | 10 (6.9) | 3 (3) |
| R5 (cmH20*s/L), mean (SD) | 3.83 ( ± 0.76) | 2.92 ( ± 0.72) |
| Abnormal R5,g n (%) | 20 (14) | 2 (2) |
| X5 (cmH20*s/L), mean (SD) | −1.09 ( ± 0.44) | −0.69 ( ± 0.25) |
| Abnormal X5 h | 10 (6.9) | 2 (2) |
Note: Available data: All 143 participants responded to all the questions except athletes regarding ICS (N = 93).
Abbreviations: 95% CI, 95% confidence interval; BMI, body mass index; ICS, inhaled corticosteroid; FeNO, fractional exhaled nitric oxide; FEV1, forced expiratory volume in one second; ppb, parts per billion; Q1, first quartile; Q3, third quartile; R5, respiratory resistance at 5 Hz; SD, standard deviation; X5, respiratory reactance at 5 Hz.
Cutoffs according to World Health Organization.
Self‐reported physician‐diagnosed with symptoms and/or medication.
Self‐reported symptom in the preceding 12 months.
Any use in the preceding 3 months.
Reference value: Global Lung Initiative.
<Lower limit of normal according to Global Lung Initiative.
>Upper limit of normal according to the reference equation by Ducharme.
<Lower limit of normal according to the reference equation by Ducharme.
3.1. Results from EIB Tests
A positive EIB test assessed by ∆FEV1 was detected in 48 participants out of 143 (33%) in non‐athletes and in 22 participants (22%) out of 98 in athletes. When assessing EIB by ∆R5, 59 participants (41%) in non‐athletes were EIB positive, while 22 athletes (22%) were EIB positive. Although there was some overlap between these two methods, a substantial number of participants were EIB‐positive only by one of the methods (Figure 1). In nonathletes, 26 participants (18%) were EIB positive by both modalities. The corresponding number was 11 participants (11%) in athletes. The coefficient of variation for the duplicate measurements of R5 at baseline was < 15% for all participants except for five participants in nonathletes, for whom the coefficient of variation was < 19%. Per group, the postexercise airway responses were as follows; in nonathletes, median (min, max) ∆FEV1 −6% (4, ‐40), ∆R5 22% (−6, 133) and, in athletes ∆FEV1 −6% (5, −25), ∆R5 10% (−18, 62).
Figure 1.

Proportion of participants EIB positive by FEV1, R5 or both methods presented per group. EIB, exercise‐induced bronchoconstriction; FEV1, forced expiratory volume in 1 s; R5, respiratory resistance at 5 Hz.
3.2. FeNO and Postexercise Airway Responses
In nonathletes, there were weak correlations between baseline log‐transformed FeNO and postexercise airway responses measured by ∆FEV1 ∆R5 and ∆X5. No such correlations were found in athletes. Spearman's rho per group and modality are presented in Figure 2.
Figure 2.

Rank correlation (Spearman's rho, r s ) between FeNO and postexercise airway response, measured by FEV1, R5 and X5 presented per group. Nonathletes in the left column and athletes in the right column. ∆FEV1 was defined as percent change from baseline to nadir postexercise. ∆R5 was defined as percent change from baseline to peak postexercise. ∆X5 was defined as change in absolute values from baseline to nadir postexercise. 95% CI, 95% confidence interval; FeNO, fractional exhaled nitric oxide; FEV1, forced expiratory volume in 1 s; R5, respiratory resistance at 5 Hz; X5, respiratory reactance at 5 Hz. [Color figure can be viewed at wileyonlinelibrary.com]
Furthermore, in nonathletes, there were associations between having elevated FeNO (≥25 ppb) and being EIB‐positive by ∆FEV1 and ∆R5; crude OR (95% CI) 2.63 (1.12–6.17) and 2.93 (1.15–7.45). In the models adjusted for height and sex the associations remained for both ∆FEV1 and ∆R5: adjusted OR (95% CI) 2.54 (1.05–6.12) and 3.05 (1.18–7.9), respectively. In athletes, no significant associations were found between having elevated FeNO and being EIB‐positive by any of the modalities (Table 2).
Table 2.
Association between elevated FeNO (≥25 ppb) and being EIB positive measured by ∆FEV1 and ∆R5 respectively. Reported as adjusted odd ratios and 95% confidence intervals, for all participants and stratified by group. The logistic regression models used were adjusted for height and sex.
| Nonathletes | Athletes | |
|---|---|---|
| EIB positive by FEV1, aOR (95%CI) | 2.54 (1.05–6.12) | 1.35 (95% CI: 0.41–4.44) |
| EIB positive by R5, aOR (95%CI) | 3.05 (1.18–7.9) | 2.06 (95% CI: 0.66–6.61) |
Note: Bold values indicate statistically significant.
Abbreviations: FeNO, fractional exhaled nitric oxide; FEV1, forced expiratory volume in 1 s; PPB, part per billion; R5, resistance at 5 Hz.
3.3. Self‐Reported Symptoms and Postexercise Airway Responses
Self‐reported wheeze was associated with ∆FEV1, ∆R5, and ∆X5 in non‐athletes. In contrast, in athletes, there were no associations between self‐reported wheeze and postexercise airway responses by any of the modalities (Table 3).
Table 3.
Associations between self‐reported symptoms and postexercise airway response measured by ∆FEV1, ∆R5, and ∆X5 respectively. Reported as β‐coefficients and 95% confidence intervals, presented by group.
| Nonathletes | Athletes | |||||
|---|---|---|---|---|---|---|
| ∆FEV1 | ∆R5 | ∆X5 | ∆FEV1 | ∆R5 | ∆X5 | |
| Wheeze | −4.00 (−6.91, −1.09) | 13.92 (4.50, 23.34) | −0.38 (−0.61, −0.15) | 0.46 (−2.20, 3.13) | −0.36 (−7.85, 7.13) | −0.03 (−0.13, 0.08) |
| EID | −4.65 (−7.65, −1.64) | 7.68 (−2.50, 17.86) | −0.21 (−0.46, 0.03) | 0.35 (−2.18, 2.88) | 1.69 (−5.53, 8.90) | −0.03 (−0.13, 0.07) |
Note: ∆FEV1 was defined as percent change from baseline to nadir postexercise. ∆R5 was defined as percent change from baseline to peak postexercise. ∆X5 was defined as change in absolute values from baseline to nadir postexercise. Bold values indicate statistically significant.
Abbreviations: EID, exercise‐induced dyspnea; FEV1, forced expiratory volume in 1 s; R5, resistance at 5 Hz; X5, reactance at 5 Hz.
In nonathletes, self‐reported EID was associated with ∆FEV1 but not ∆R5 or ∆X5. In athletes, no associations were found between EID and postexercise airway responses by any of the modalities (Table 3).
4. Discussion
In this study of postexercise airway responses measured by spirometry and oscillometry in nonathlete and athlete adolescents, we found a substantial number of participants being EIB‐positive by one of the modalities. However, both groups had only a modest overlap between EIB defined by spirometry and oscillometry. In nonathletes but not in athletes, FeNO and self‐reported respiratory symptoms were associated with postexercise airway responses measured by spirometry and oscillometry. Only in nonathletes did elevated FeNO increase the likelihood of being EIB‐positive as determined by spirometry or oscillometry.
Baseline FeNO, ∆FEV1, and ∆R5 showed weak significant correlations among nonathletes, while no correlations were observed in athletes. To our knowledge, this is the first population‐based study to investigate FeNO and postexercise airway response, measured by both spirometry and oscillometry. In children with asthma or with a high risk of asthma, baseline FeNO has been reported to correlate with postexercise airway response measured by ∆FEV1 [26]. Previous studies of FeNO and postexercise oscillometric indices are scarce. Our results indicate that FeNO is associated with the magnitude of bronchoconstriction measured by both modalities, but only in nonathletes. Similar to the nonathletes in this study, Malmberg and colleagues have reported a relationship between FeNO and severity of EIB assessed by oscillometry in young wheezy children [31].
When analyzing elevated FeNO ( ≥ 25 ppb) as a predictor for EIB, elevated FeNO was associated with EIB defined by both spirometry and oscillometry only in nonathletes. In athletes, elevated FeNO was not associated with EIB defined by any of the modalities. It has been reported previously that FeNO can predict EIB defined by spirometry in schoolchildren with asthma or suspected asthma [25], while in athletes, the value of elevated FeNO as a predictor of EIB is reported to be low [28]. In contrast, in a recent study of adolescent athletes, Goossens et al. found that elevated FeNO was an independent predictor of EIB and that FeNO levels were correlated with the severity of EIB in atopic athletes [32]. These findings suggest that different underlying mechanisms may contribute to EIB in atopic versus non‐atopic athletes. Indeed, differences in the EIB phenotype, type‐2 or non‐type‐2 inflammation, may account for the discordance between the two groups in the present study. Previous research has shown that a large proportion of athletes with EIB have non‐type‐2 inflammation and hence a low expected FeNO [33] whereas EIB has been connected to type‐2 inflammation in the general population [34].
In nonathletes, reporting wheeze was negatively associated with ∆FEV1 and ∆X5, and positively associated with ∆R5. EID was negatively associated with ∆FEV1 in the same group, but no associations were found between EID and the oscillometric indices. This observation implies that wheeze may be linked to a more pronounced postexercise response in the peripheral airways, detected only by oscillometry. In line with this, oscillometric indices have previously been reported to relate to respiratory symptoms in individuals with normal spirometry in a large population‐based middle‐aged cohort [17]. In athletes, we found no associations between wheeze or EID and either modality. In children and adolescents referred for evaluation of exertional dyspnea [35] and in several studies of athletes [13] self‐reported symptoms have been reported to be poor predictors of EIB measured by ∆FEV1. Our results suggest that postexercise airway responses measured by oscillometry display a similar pattern as spirometry, showing some associations in non‐athletes and no associations with symptoms in athletes. This underscores that a diagnosis of EIB should not be based on self‐reported respiratory symptoms alone, without objective evidence of bronchoconstriction after an airway challenge [6].
EIB defined by ∆FEV1 and ∆R5, respectively, showed a modest overlap in these two cohorts. About half of the participants who were positive by ∆FEV1 were also positive by ∆R5, while less than half of the participants who were positive by ∆R5 were also positive by ∆FEV1. Although the two methods are measures of airway obstruction, the measurements are performed at different lung volumes and may reflect changes at different levels of the respiratory system, thus perhaps recognizing different subtypes of EIB [36]. The modest overlap between ∆FEV1 and ∆R5 for diagnosing EIB is in line with previous studies in adult athletes [23], and in a previous study by our group in adolescents [22]. In contrast, in individuals with asthma or with suspected asthma, post‐challenge oscillometric indices have been reported to show high agreement with EIB defined by ∆FEV1 [19, 20, 21]. Differences in population selection, severity of bronchoconstriction, and diagnostic thresholds may account for the diverging results.
The diagnostic thresholds for EIB applied in the present study were ∆FEV1 ≤ −10% or ∆R5 ≥ 25% at any time point postexercise. The threshold for ∆FEV1 ≤ −10% is widely accepted for diagnosing EIB after an exercise challenge [10], while robust recommendations for corresponding thresholds for ∆R5 are scarce, and cutoff values ranging from 14% to 50% have been suggested in previous studies [18, 21, 23]. Given the broad range of the suggested cutoff values postexercise, the threshold of ∆R5 ≥ 25% used in the current study is also informed by earlier research on the oscillometric response to various bronchial challenges and bronchodilator treatments. Schulze and colleagues reported that a 45% increase in R5 was associated with a 20% reduction in FEV1 during a methacholine challenge [37]. Similarly, Oostveen and colleagues found that a 32% decrease in R5 indicated a significant bronchodilator response in adults aged 18–80 years [38], a result consistent with the findings by Johansson and colleagues, where a 29% decrease in R5 was found to be a significant bronchodilator response in middle‐aged adults [39].
5. Strengths and Limitations
The strengths of this study include the random selection of participants from two relatively large adolescent population‐based study cohorts, the standardized objective exercise challenge using dry air, and the postexercise airway responses measured by both spirometry and oscillometry.
Yet, there are some limitations that need to be addressed. Wheeze and EID were self‐reported in a questionnaire, and the participant's interpretation of the questions might have affected their answers. Information on atopic status would have been of value to describe the study population further. Oscillometry was performed before spirometry at each time point, but an influence on bronchial tone by the forced expirations during spirometry cannot be completely ruled out. Due to frequent measurements and short time intervals between each measurement, single oscillometry measurements were performed postexercise, although triplicate measurements are recommended. However, in epidemiological research, one measurement has been proposed to suffice [40].
6. Conclusion
For adolescents who are not high‐level athletes, elevated FeNO or reports of wheezing or EID may guide clinicians in selecting those who should be referred for EIB testing. In contrast, for adolescent athletes, FeNO levels and reports of wheezing or EID appear to offer limited guidance, making access to objective testing essential.
Spirometry and oscillometry for assessing exercise‐induced bronchoconstriction do not perfectly align, suggesting that the two methods may detect different locations of airway narrowing. Therefore, oscillometry could serve as a complementary tool to spirometry when evaluating abnormal airway responses after exercise. However, further research is needed to establish appropriate diagnostic thresholds for postexercise responses by oscillometric indices and the added clinical value.
Author Contributions
Karin Ersson: investigation, writing – original draft, data curation, methodology, project administration, formal analysis, visualization, writing – review and editing. Kjell Alving: conceptualization, writing – review and editing, resources, methodology. Margareta Emtner: writing – review and editing, conceptualization. Christer Janson: writing – review and editing, resources, conceptualization. Henrik Johansson: writing – review and editing, conceptualization, supervision, data curation, investigation, funding acquisition, methodology. Andrei Malinovschi: conceptualization, funding acquisition, methodology, supervision, resources, writing – review and editing, investigation, software.
Ethics Statement
All participants signed a written informed consent form at inclusion in the study. For participants under 15, informed consent was also obtained from all guardians. The ethical review board in Uppsala, Sweden, provided ethical approval for this study (Dnr 2011/413 and Dnr 2016/169).
Conflicts of Interest
Kjell Alving reports receiving personal payment, equipment, and material for a clinical study outside of the present manuscript from NIOX. Andrei Malinovschi has received lecture and/or advisory board fees from Boehringer Ingelheim and Chiesi outside the submitted study as well as in‐kind support in form of nitric oxide sensors from NIOX (a producer of FeNO devices) within a frame of an investigator‐initiated study (not the present study). The other authors declare no conflicts of interest.
Acknowledgments
This study was sponsored by the Swedish Heart and Lung Foundation (grant 20110179), the Swedish Asthma and Allergy Association (grant F2017‐0010), the Signhild Engqvist Foundation, the Bror Hjerpstedt Foundation, the Gillbergska Foundation and the Uppsala County Association against Heart and Lung Diseases.
Ersson K., Alving K., Emtner M., Janson C., Johansson H., and Malinovschi A., “Postexercise Airway Responses by Spirometry and Oscillometry in Nonathlete and Athlete Adolescents,” Pediatric Pulmonology 60 (2025): 1‐9, 10.1002/ppul.71296.
Henrik Johansson and Andrei Malinovschi contributed equally to this study.
Data Availability Statement
The ethical approval does not allow the authors to make all the data publicly available, according to Swedish law. Unidentified data that supports the findings of this study are available upon reasonable request from the authors.
References
- 1. Johansson H., Norlander K., Hedenström H., et al., “Exercise‐Induced Dyspnea Is a Problem Among the General Adolescent Population,” Respiratory Medicine 108, no. 6 (2014): 852–858. [DOI] [PubMed] [Google Scholar]
- 2. Yeatts K., Johnston Davis K., Peden D., and Shy C., “Health Consequences Associated With Frequent Wheezing in Adolescents Without Asthma Diagnosis,” European Respiratory Journal 22, no. 5 (2003): 781–786. [DOI] [PubMed] [Google Scholar]
- 3. Turcotte H., Langdeau J.‐B., Thibault G., and Boulet L.‐P., “Prevalence of Respiratory Symptoms in an Athlete Population,” Respiratory Medicine 97, no. 8 (2003): 955–963. [DOI] [PubMed] [Google Scholar]
- 4. Ersson K., Mallmin E., Malinovschi A., Norlander K., Johansson H., and Nordang L., “Prevalence of Exercise‐Induced Bronchoconstriction and Laryngeal Obstruction in Adolescent Athletes,” Pediatric Pulmonology 55, no. 12 (2020): 3509–3516. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5. Halvorsen T., Walsted E. S., Bucca C., et al., “Inducible Laryngeal Obstruction: An Official Joint European Respiratory Society and European Laryngological Society Statement,” European Respiratory Journal 50, no. 3 (2017): 1602221. [DOI] [PubMed] [Google Scholar]
- 6. Parsons J. P., Hallstrand T. S., Mastronarde J. G., et al., “An Official American Thoracic Society Clinical Practice Guideline: Exercise‐Induced Bronchoconstriction,” American Journal of Respiratory and Critical Care Medicine 187, no. 9 (2013): 1016–1027. [DOI] [PubMed] [Google Scholar]
- 7. Gaillard E. A., Kuehni C. E., Turner S., et al., “European Respiratory Society Clinical Practice Guidelines for the Diagnosis of Asthma in Children Aged 5–16 Years,” European Respiratory Journal 58, no. 5 (2021): 2004173. [DOI] [PubMed] [Google Scholar]
- 8. Aggarwal B., Mulgirigama A., and Berend N., “Exercise‐Induced Bronchoconstriction: Prevalence, Pathophysiology, Patient Impact, Diagnosis and Management,” NPJ Primary Care Respiratory Medicine 28, no. 1 (2018): 31. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9. Price O. J., Sewry N., Schwellnus M., et al., “Prevalence of Lower Airway Dysfunction in Athletes: A Systematic Review and Meta‐Analysis by a Subgroup of the IOC Consensus Group on ‘Acute Respiratory Illness in the Athlete’,” British Journal of Sports Medicine 56, no. 4 (2022): 213–222. [DOI] [PubMed] [Google Scholar]
- 10. Hallstrand T. S., Leuppi J. D., Joos G., et al., “Ers Technical Standard on Bronchial Challenge Testing: Pathophysiology and Methodology of Indirect Airway Challenge Testing,” European Respiratory Journal 52, no. 5 (2018): 1801033. [DOI] [PubMed] [Google Scholar]
- 11. Christensen P. M., Thomsen S. F., Rasmussen N., and Backer V., “Exercise‐Induced Laryngeal Obstructions: Prevalence and Symptoms in the General Public,” European Archives of Oto‐Rhino‐Laryngology 268, no. 9 (2011): 1313–1319. [DOI] [PubMed] [Google Scholar]
- 12. Johansson H., Norlander K., Berglund L., et al., “Prevalence of Exercise‐Induced Bronchoconstriction and Exercise‐Induced Laryngeal Obstruction in a General Adolescent Population,” Thorax 70, no. 1 (2015): 57–63. [DOI] [PubMed] [Google Scholar]
- 13. Price O. J., Hull J. H., Ansley L., Thomas M., and Eyles C., “Exercise‐Induced Bronchoconstriction in Athletes—A Qualitative Assessment of Symptom Perception,” Respiratory Medicine 120 (2016): 36–43. [DOI] [PubMed] [Google Scholar]
- 14. King G. G., Bates J., Berger K. I., et al., “Technical Standards for Respiratory Oscillometry,” European Respiratory Journal 55, no. 2 (2020): 1900753. [DOI] [PubMed] [Google Scholar]
- 15. Kaminsky D. A., Simpson S. J., Berger K. I., et al., “Clinical Significance and Applications of Oscillometry,” European Respiratory Review 31, no. 163 (2022): 210208. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16. Takeda T., Oga T., Niimi A., et al., “Relationship Between Small Airway Function and Health Status, Dyspnea and Disease Control in Asthma,” Respiration 80, no. 2 (2010): 120–126. [DOI] [PubMed] [Google Scholar]
- 17. Qvarnström B., Engström G., Frantz S., et al., “Impulse Oscillometry Indices in Relation to Respiratory Symptoms and Spirometry in the Swedish Cardiopulmonary Bioimage Study,” ERJ Open Research 9, no. 5 (2023): 00736‐2022. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18. Malmberg L. P., Mäkelä M. J., Mattila P. S., Hammarén‐Malmi S., and Pelkonen A. S., “Exercise‐Induced Changes in Respiratory Impedance in Young Wheezy Children and Nonatopic Controls,” Pediatric Pulmonology 43, no. 6 (2008): 538–544. [DOI] [PubMed] [Google Scholar]
- 19. Barreto M., Veneroni C., Caiulo M., et al., “Within‐Breath Oscillometry for Identifying Exercise‐Induced Bronchoconstriction in Pediatric Patients Reporting Symptoms With Exercise,” Frontiers in Pediatrics 11 (2023): 1324413. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20. Evans T. M., Rundell K. W., Beck K. C., Levine A. M., and Baumann J. M., “Impulse Oscillometry Is Sensitive to Bronchoconstriction After Eucapnic Voluntary Hyperventilation or Exercise,” Journal of Asthma 43, no. 1 (2006): 49–55. [DOI] [PubMed] [Google Scholar]
- 21. Seccombe L. M., Peters M. J., Buddle L., and Farah C. S., “Exercise‐Induced Bronchoconstriction Identified Using the Forced Oscillation Technique,” Frontiers in Physiology 10 (2019): 1411. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22. Veneroni C., Pompilio P. P., Alving K., et al., “Self‐Reported Exercise‐Induced Dyspnea and Airways Obstruction Assessed by Oscillometry and Spirometry in Adolescents,” Pediatric Allergy and Immunology 33, no. 1 (2022): e13702. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23. Price O. J., Ansley L., Bikov A., and Hull J. H., “The Role of Impulse Oscillometry in Detecting Airway Dysfunction in Athletes,” Journal of Asthma 53, no. 1 (2016): 62–68. [DOI] [PubMed] [Google Scholar]
- 24. Horváth I., Barnes P. J., Loukides S., et al., “A European Respiratory Society Technical Standard: Exhaled Biomarkers in Lung Disease,” European Respiratory Journal 49, no. 4 (2017): 1600965. [DOI] [PubMed] [Google Scholar]
- 25. Buchvald F., Hermansen M. N., Nielsen K. G., and Bisgaard H., “Exhaled Nitric Oxide Predicts Exercise‐Induced Bronchoconstriction in Asthmatic School Children,” Chest 128, no. 4 (2005): 1964–1967. [DOI] [PubMed] [Google Scholar]
- 26. Schoos A. M. M., Christiansen C. F., Stokholm J., Bønnelykke K., Bisgaard H., and Chawes B. L., “FeNO and Exercise Testing in Children at Risk of Asthma,” Journal of Allergy and Clinical Immunology: In Practice 6, no. 3 (2018): 855–862.e2. [DOI] [PubMed] [Google Scholar]
- 27. Johansson H., Norlander K., Alving K., et al., “Exercise Test Using Dry Air in Random Adolescents: Temporal Profile and Predictors of Bronchoconstriction,” Respirology 21, no. 2 (2016): 289–296. [DOI] [PubMed] [Google Scholar]
- 28. Dickinson J., Gowers W., Sturridge S., et al., “Fractional Exhaled Nitric Oxide in the Assessment of Exercise‐Induced Bronchoconstriction: A Multicenter Retrospective Analysis of UK‐Based Athletes,” Scandinavian Journal of Medicine & Science in Sports 33, no. 7 (2023): 1221–1230. [DOI] [PubMed] [Google Scholar]
- 29. ATS/ERS Recommendations for Standardized Procedures for the Online and Offline Measurement of Exhaled Lower Respiratory Nitric Oxide and Nasal Nitric Oxide, 2005,” American Journal of Respiratory and Critical Care Medicine 171, no. 8 (2005): 912–930, https://www.atsjournals.org/doi/abs/10.1164/rccm.200406-710ST. [DOI] [PubMed] [Google Scholar]
- 30. Miller M. R., Hankinson J., Brusasco V., et al., “Standardisation of Spirometry,” European Respiratory Journal 26, no. 2 (2005): 319–338. [DOI] [PubMed] [Google Scholar]
- 31. Malmberg L. P., Pelkonen A. S., Mattila P. S., Hammarén‐Malmi S., and Mäkelä M. J., “Exhaled Nitric Oxide and Exercise‐Induced Bronchoconstriction in Young Wheezy Children – Interactions With Atopy,” Pediatric Allergy and Immunology 20, no. 7 (2009): 673–678. [DOI] [PubMed] [Google Scholar]
- 32. Goossens J., Vandekerckhove J., Jonckheere A. C., et al., “Exercise‐Induced Bronchoconstriction in Adolescent Recreational Athletes: Potential Screening Strategies,” Pediatric Allergy and Immunology 35, no. 8 (2024): e14220. [DOI] [PubMed] [Google Scholar]
- 33. Couto M., Kurowski M., Moreira A., et al., “Mechanisms of Exercise‐Induced Bronchoconstriction in Athletes: Current Perspectives and Future Challenges,” Allergy 73, no. 1 (2018): 8–16. [DOI] [PubMed] [Google Scholar]
- 34. Sverrild A., Porsbjerg C., Thomsen S. F., and Backer V., “Airway Hyperresponsiveness to Mannitol and Methacholine and Exhaled Nitric Oxide: A Random‐Sample Population Study,” Journal of Allergy and Clinical Immunology 126, no. 5 (2010): 952–958. [DOI] [PubMed] [Google Scholar]
- 35. Abu‐Hasan M., Tannous B., and Weinberger M., “Exercise‐Induced Dyspnea in Children and Adolescents: If Not Asthma then What?,” Annals of Allergy, Asthma & Immunology 94, no. 3 (2005): 366–371. [DOI] [PubMed] [Google Scholar]
- 36. Marchal F., Schweitzer C., and Thuy L., “Forced Oscillations, Interrupter Technique and Body Plethysmography in the Preschool Child,” Paediatric Respiratory Reviews 6, no. 4 (2005): 278–284. [DOI] [PubMed] [Google Scholar]
- 37. Schulze J., Smith H. J., Fuchs J., et al., “Methacholine Challenge in Young Children as Evaluated by Spirometry and Impulse Oscillometry,” Respiratory Medicine 106, no. 5 (2012): 627–634. [DOI] [PubMed] [Google Scholar]
- 38. Oostveen E., Boda K., van der Grinten C. P. M., et al., “Respiratory Impedance in Healthy Subjects: Baseline Values and Bronchodilator Response,” European Respiratory Journal 42, no. 6 (2013): 1513–1523. [DOI] [PubMed] [Google Scholar]
- 39. Johansson H., Wollmer P., Sundström J., Janson C., and Malinovschi A., “Bronchodilator Response in FOT Parameters in Middle‐Aged Adults From SCAPIS: Normal Values and Relationship to Asthma and Wheezing,” European Respiratory Journal 58, no. 3 (2021): 2100229. [DOI] [PubMed] [Google Scholar]
- 40. Wollmer P., Tufvesson E., Wennersten A., et al., “Within‐Session Reproducibility of Forced Oscillometry,” Clinical Physiology and Functional Imaging 41, no. 5 (2021): 401–407. [DOI] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
The ethical approval does not allow the authors to make all the data publicly available, according to Swedish law. Unidentified data that supports the findings of this study are available upon reasonable request from the authors.
