Edited by: Tim Takken, University Medical Center Utrecht, Netherlands
Reviewed by: Jérémie F. Cohen, Necker-Enfants Malades Hospital, France; Erik Hulzebos, University Medical Center Utrecht, Netherlands
This article was submitted to General Pediatrics and Pediatric Emergency Care, a section of the journal Frontiers in Pediatrics
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Exercise-induced bronchoconstriction (EIB) is defined as an acute narrowing of the airways that occurs as a result of exercise (
However, it is unclear if this approach is sufficient to properly assess EIB in children. Several studies have shown a poor relation between reported exercise-related symptoms in children and EIB as measured with an ECT (
This study had a cross-sectional design. Children 6–17 years old with pediatrician diagnosed asthma were recruited from the outpatient clinic of the pediatric department of Medisch Spectrum Twente, Enschede, The Netherlands from May 2015 to July 2015. Children with spirometry-induced bronchoconstriction or severe airflow limitation in baseline spirometry, defined as a forced expiratory volume in 1 s (FEV1) < 60% of predicted, were not included. None used short- or long-acting bronchodilators for at least 24 h before the exercise challenge test. Children with other pulmonary or cardiac disorders were excluded. A STARD checklist (
The clinical assessments and ECT's were performed at OCON sport, in Hengelo. This was carried out by two healthcare professionals, one sports-physician, and one pediatric pulmonologist, with both extensive experience in the clinical assessment of asthma and EIB.
Before the start of the ECT, a medical history with specific focus on asthma symptoms was obtained (
Elements of medical history and physical examination
General asthma symptoms |
Exercise-induced symptoms |
Nocturnal symptoms |
Nasal symptoms |
Atopy |
Family history positive for asthma |
Medication use |
General impression |
Nasal obstruction |
Nasal crease (allergic salute) |
Vesicular breath sounds |
Inspiratory stridor |
Expiratory wheezing |
Position of patient and camera while recording.
The ECT's were performed in a climate chamber with cold (10.0–12.0°C), dry air following standard protocol (
Classification of EIB severity
No EIB | <10% |
Mild EIB | >10% but <25% |
Moderate EIB | >25% but <50% |
Severe EIB | >50% for steroid-naïve patients |
The ECT results were interpreted by the above mentioned healthcare professionals.
Twenty pediatricians from three different teaching hospitals (Medisch Spectrum Twente, Isala Klinieken Zwolle, ZGT Almelo/Hengelo) participated in this study. Their average years of experience was 14.4 years (SD 9.8) and two pediatrician were subspecialized as pediatrician-pulmonologist. Each pediatrician independently evaluated five children that were randomly assigned to him or her, providing 100 evaluations in total. The evaluation procedure consisted of two steps.
First, occurrence and severity of EIB (
Results were expressed as mean values ± standard deviation (SD) for the normally distributed continuous data and as median ± interquartile range (IQR) for not-normally distribute data. For nominal or ordinal data, numbers with corresponding percentages were used. The maximum fall in FEV1 as a percentage of predicted was calculated and used for statistical analyses.
Sensitivity was calculated as the proportion of children with EIB, diagnosed with an ECT as reference standard, who were given an EIB diagnosis by the pediatricians based on the provided clinical information and spirometry results. Specificity was calculated as the proportion of children without EIB, who were not given an EIB diagnosis by the pediatricians.
The 95% confidence intervals (CI) for sensitivity and specificity were calculated using Episheet (
To assess the degree of concordance between the prediction of EIB severity by the pediatricians and the validated classification of EIB based on the ECT, a linear weighted Cohen's Kappa was calculated. Cohen's Kappa values were classified as: <0 = poor; 0–0.2 = slight; 0.2–0.4 = fair; 0.4–0.6 = moderate; 0.6–0.8 = substantial; 0.8–1.0 = almost perfect (
For these analysis all 100 evaluations were included, acknowledging the fact that each child was present multiple times in the dataset, albeit assessed by different pediatricians.
A two-sided
This study was approved by the Medical Ethics Review Board Twente. All children and parents/guardians received written patient information and provided written informed consent before participating in the study.
Of 24 children with usable consultation videos, three children had spirometry-induced bronchoconstriction, and one child used salbutamol shortly before the ECT. Twenty children completed the protocol and were included for statistical analyses. Twenty pediatricians independently assessed five children, providing a total of 100 assessments.
Baseline characteristics of the study sample [10 boys (50.0%)] are shown in
Characteristics of the study sample (
Female | 10 (50.0%) |
Male | 10 (50.0%) |
Age, years | 11.6 (3.4) |
BMI, kg/m2 | 19.5 (4.6) |
Atopy |
11 (55.0%) |
SABA | 13 (65%) |
LABA | 2 (10%) |
ICS | 10 (50%) |
LTRA | 6 (30%) |
NCS | 5 (25%) |
Exercise-induced symptoms | 8 (40.0%) |
FEV1 predicted, % | 92.7 (13.9) |
Fall in |
15.1 (1.2–65.1) |
No EIB (<10%) | 9 (45.0%) |
Mild EIB (10–25%) | 4 (20.0%) |
Moderate EIB (25–50%) | 2 (10.0) |
Severe EIB (>50% or ICS use with >30%) | 5 (25.0) |
Reversibility |
18.9 (−11.0–62.3) |
EIB occurrence after the ECT was compared with the predicted occurrence of EIB by pediatricians (
EIB occurrence after the exercise challenge test compared to the predicted occurrence of EIB.
No | 11 | 9 | 20 | |
Yes | 34 | 46 | 80 | |
Total | 45 | 55 | 100 |
Overview of predicted and tested EIB severity classifications in participants.
EIB prediction by pediatricians based on CA | No EIB | 11 | 5 | 1 | 4 | 21 |
Mild EIB | 22 | 10 | 13 | 6 | 51 | |
Moderate EIB | 10 | 5 | 8 | 2 | 25 | |
Severe EIB | 2 | 0 | 1 | 0 | 3 | |
Total | 45 | 20 | 23 | 12 | 100 | |
EIB prediction by pediatricians based on CA + spirometry | No EIB | 11 | 5 | 1 | 3 | 20 |
Mild EIB | 21 | 11 | 8 | 3 | 43 | |
Moderate EIB | 10 | 4 | 11 | 5 | 30 | |
Severe EIB | 3 | 0 | 3 | 1 | 7 | |
Total | 45 | 20 | 23 | 12 | 100 |
The agreement between the EIB classifications is shown in
Agreement between pediatricians' prediction of EIB severity and EIB severity after an ECT.
Clinical assessment |
0.05 (0.00–0.17) | |
Clinical assessment + spirometry * ECT | 0.19 (0.06–0.32) |
Differences between the paired EIB severity classifications, analyzed with the McNemar test, are shown in
Differences between pediatricians' prediction of EIB severity and EIB severity after an ECT.
Clinical assessment * clinical assessment + spirometry | |
Clinical assessment * ECT | |
Clinical assessment + spirometry * ECT |
This study aimed to evaluate the capacity of pediatricians to predict the occurrence and severity of EIB based on information routinely available during an outpatient clinic visit. In 100 evaluations, the sensitivity of a pediatricians' predicted diagnosis of EIB was 84%, compared to a specificity of 24%.
The prediction of EIB severity based on a clinical assessment including a medical history, physical examination, and video images of the assessment was poor, with an underestimation of EIB severity in children with moderate and severe EIB. This prediction remained poor when pediatricians were informed about pre-exercise pulmonary function.
To our knowledge, this is the first study that focused on the capacity of pediatricians to predict EIB based on merged data, rather than focusing on separate aspects, available during a routine clinical visit. Our results are in line with previous research that found that clinical information alone is unreliable to predict EIB, leading to both over- and underestimation.
Seear et al. (
Four studies found no relationship between pre-exercise spirometry values and EIB in children (
Studies focusing on athletes with EIB are in line with our results. Hallstrand et al. (
The unreliability of only using symptoms for the assessment of asthma control was demonstrated by Shefer et al. (
A major strength of this study is the standardized exercise challenge tests that were performed in a climate chamber with cold and dry air, following standard protocol. Young children (6–7 years old) performed the test on a jumping castle, a method that has previously been validated by members of our study group (
The main limitation of our study is that pediatricians predicted occurrence and severity of EIB based on clinical information not personally obtained. This information was obtained by the investigators of this study during the clinical assessments and ECT's. The pediatricians received this information afterwards and each assessed five children based on the provided information. We complemented this information with video images of the children so that the pediatricians could form a general impression of the children. This study setting is however not a perfect simulation of a real-life setting, and therefore could have led to a less accurate prediction of EIB by the pediatricians.
Another limitation of our study is the inflated sample size: 20 pediatricians each assessed five children (from a total study group of 20 children), providing 100 evaluations. We also acknowledge that therefore each child was present multiple times in our dataset, albeit assessed by different pediatricians.
In conclusion, this study shows that the clinical prediction of EIB occurrence by pediatricians is sensitive, but poorly specific. Furthermore, the prediction of EIB severity based on information routinely available during an outpatient clinic visit is poor. Pediatricians should be aware of this unreliability to prevent misjudgement of asthma control by evaluating EIB without an ECT.
This study was approved by the Medical Ethics Review Board Twente. All children and parents/guardians received written patient information and provided written informed consent before participating in the study. This study was registered on the Dutch Trial Registration under number NTR 5534 (
All except MB-K and JvdP contributed to data acquisition. NL, MB-K, and JvdP contributed to the data analysis. All authors contributed equally on the research protocol, the writing and editing of the manuscript.
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
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