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1 Institute of Environmental Medicine, and 2 Sachs' Children's Hospital, Sodersjukhuset, Karolinska Institutet, and 3 Dept of Environmental Health, Stockholm County Council, Stockholm, Sweden
CORRESPONDENCE: P. Thunqvist, Institute of Environmental Medicine, Karolinska Institutet, Box 210, SE - 171 77, Stockholm, Sweden. Fax: 46 8304571. E-mail: per.thunqvist@sachsska.sos.sll.se
Keywords: asthma, ice hockey, indoor ice arena, nitrogen dioxide, rhinitis
Received: August 12, 2001
Accepted December 25, 2001
This study was supported by grants from the Swedish Foundation of Strategic and Environmental Research (MISTRA) and the Asthma and Allergy Association of Sweden.
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Abstract |
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Children regularly playing hockey in the arenas (nine propane, six electric) were sent a questionnaire, including questions on allergic disease and risk factors. Measurements of NO2 were performed with passive diffusion samplers during 3 consecutive days.
The mean NO2 concentration in the propane arenas was 276 µg·m–3 (range 28–1015 µg·m–3) and 11 µg·m–3 (2–30) in the electric arenas. Questionnaires were answered by 1,536 children (78%), with an overall prevalence of asthma of 16%. The odds ratio (OR) for asthma was 0.9 (95% confidence interval (CI) 0.7–1.2) comparing propane arenas to electric. However, children in propane arenas with higher than median concentration of NO2 reported more wheezing (OR 1.4, 95% CI 1.0–1.9) and nasal symptoms (OR 1.7, 95% CI 1.3–2.3) than children in propane arenas with lower concentrations.
In conclusion, children playing ice hockey in indoor arenas have a high prevalence of asthma, but it appears unlikely that increased exposure to combustion products, including nitrogen dioxide, is a major contributor to this excess risk.
Long-term exposure to ambient air pollution and its potential effect on the development of asthma and atopy has been a topic of interest in recent years. Some authors report an association between increased exposure to air pollution, with nitrogen dioxide (NO2) as a major component, and respiratory tract illness as well as atopy in children, but the evidence is not consistent 1–5. In these studies the contrast in exposure to NO2 between study subjects was limited and together with potential confounding this makes the results difficult to interpret.
High concentrations of NO2 may occur in ice arenas when propane- or gasoline-powered ice-resurfacing machines are used 6. Outbreaks of respiratory illness have been reported after exposure to very high concentrations of NO2 in ice arenas, i.e. in the order of several thousands of µg·m–3, probably due to malfunctioning of combustion engines and poor ventilation 7, 8. In follow-up investigations after such accidents no long-term health effects have been demonstrated 7, 8. However, there is a lack of studies on long-term effects of regular exposure to high NO2 concentrations in ice arenas.
The aim of this study was to assess the risk of bronchial asthma for children playing ice hockey or figure skating in indoor ice arenas with propane-powered ice-resurfacing machines compared to a group of children primarily attending arenas with electric-powered machines.
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Material and methods |
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TOPAbstractMaterial and methodsResultsDiscussionAcknowledgementsReferences |
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67,000 inhabitants. Thus, 15 arenas at 14 different locations were included, nine using propane-powered and six using electric-powered machines. Two of the electric-powered arenas were located in the city of Gävle.
Study population
All children in hockey and figure-skating clubs in Sweden are registered from the age of 10 in a mandatory insurance file. From this file it was possible to identify 2,231 children, aged 10–16 yrs who were presently active in clubs using the selected arenas or had been active during any of the 3 yrs prior to the study. In the winter of 1999 a questionnaire was sent to the selected children and their parents. The response rate following two postal reminders was 77.8%, similar for children attending electric-powered and propane-powered arenas. One hundred and nine of the children who attended electric arenas reported that their main activity was on outdoor rinks and were excluded from analysis. Furthermore, children in electric arenas with mixed exposure to both types of resurfacing machines were also excluded, leaving a total of 1,535 children for the final analysis.
Questionnaire and health outcome measurements
The questionnaire had 57 questions, including 10 on symptoms of atopic diseases identical to those in the International Study of Asthma and Allergies in Childhood (ISAAC-1) for children aged 13–14 yrs 9. Furthermore, questions on "physician-diagnosed asthma" and asthma medication were added. To estimate the exposure to NO2, questions on physical exercise in ice arenas, training intensity and use of more than one arena were included. Questions on living conditions, household pets (past and present), household smoking (past and present) and parental history of allergic disease were also included. The parents were given instructions to complete the questionnaire together with their child.
Nitrogen dioxide monitoring
At the time of distribution of the questionnaires ambient NO2 was measured inside and outside all the selected arenas. In addition to the propane- or electric-powered resurfacing machines, all arenas used ice edgers powered by combustion engines. The resurfacing machines were used daily on average 1 h and the edgers were usually used once or twice a week for 15 min. The measurements were started on the day before the "special ice-care day", when the resurfacing machine was operated for a longer time and the edger was used. NO2 concentrations were determined by passive diffusion samplers at three different locations in each arena during 3 consecutive days. Each sampler was in use for 1 day only. At each arena two samplers were located near the rink (goal and rink-side) and one outside.
The samplers were in position during open hours, usually 13 h·day–1. To control for passive diffusion of NO2 into the sampler when not used, a control sampler not removed from its sealed tube was used during all 3 days in each arena. The sampler was developed by the Swedish Environment Research Institute and gives time integrated NO2 concentrations 10. The relative sd between duplicate samplers has been estimated as <4% and the concentrations are within ±15% of those obtained by volumetric techniques.
Statistical analysis
Comparisons between children exposed to propane-powered and electric-powered resurfacing machines were performed by estimating odds ratios (OR) and 95% confidence intervals (CI), using logistic regression analysis. Adjustment was made for sex and family history of allergic disease. Other potential confounders, such as keeping furred pets, a smoking mother or condensation on window panes during wintertime, did not influence the OR and were not included in the regression models. Individuals not responding to a particular question were excluded from analysis of that question. However, missing values were 
1% in any single question.
Ethical considerations
The Ethics Committee of Karolinska Institute, Stockholm, Sweden, approved the study and all families gave informed consent before participation.
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Results |
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. The age and sex distribution as well as training history were similar in the two groups of children. Most children had >3 yrs of activity in the ice arenas and 79% (propane arenas) and 76% (electric arenas) were still active in the winter of 1999 when the present study was performed. Of the 328 children who had stopped sport activities in ice arenas during the last 3 yrs, change of sports was reported as the main reason (78%). This was equally distributed between the two groups. However, 10 children reported breathing problems when attending ice arenas (four propane, six electric) as the major cause. There was no significant difference in potential risk factors for bronchial asthma between groups, such as housing conditions, indoor dampness, parental smoking (past or present) or keeping furred pets (past or present). However, children in the electric-arena group tended to have a higher prevalence of parental history of asthma and atopy (41.9%) than children in the propane-arena group (38.7%).
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. There was a wide range of NO2 concentrations in the nine propane arenas (28–1,015 µg·m–3). The measurements were consistent within the arenas, i.e. the range of NO2 was small in each arena. The same arena had the lowest concentrations on all 3 consecutive days and another arena had the highest levels during all 3 days. The mean and median values were higher on the second and third day in most arenas due to longer use of resurfacing and ice-edger machines on the second or third day. The mean indoor concentrations were >20-fold higher than the mean outdoors when propane-powered resurfacing machines had been used. The highest NO2 concentrations in the electric arenas were similar to the lowest in the propane arenas. Outdoor NO2 concentrations tended to be similar to those inside the electric arenas.
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). Most children with "ever asthma" had their onset of asthma before starting hockey training or figure skating in ice arenas (63% attending propane arenas, 58% attending electric arenas). When these children were excluded there was still no difference in symptom prevalence between the two exposure groups. Remission of asthma, expressed as "ever asthma" but without current symptoms of asthma and/or asthma medication during the past year, was also similar among children practising in electric arenas (16%) and in propane arenas (13%).
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). Four of the propane arenas had NO2 concentrations above the median of NO2 (mean 510 µg·m–3, median 396 µg·m–3). The remaining nine arenas had a mean concentration of 89 µg·m–3 and a median concentration of 65 µg·m–3. Thirteen subjects attended propane arenas without known concentrations of NO2 and are excluded from this subanalysis. Nasal symptoms, without upper respiratory infection and "ever wheeze" were more prevalent among children with high exposure levels of NO2. There was also a tendency to increased prevalence of "ever asthma", physician-diagnosed asthma and symptoms of asthma in the high exposure group. The onset of asthma before beginning to attend ice arenas regularly was similar in the two exposure groups (low 63%, high 62%). There was no significant difference in years of indoor hockey activities, training intensity and/or potential risk factors for development of atopic disease among children in the high and low NO2-exposure groups.
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Discussion |
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Inhalation of extremely high concentrations of NO2 can induce toxic pneumonitis and pulmonary oedema. Controlled exposure studies show an increased bronchial hyperresponsiveness in normal subjects at concentrations >2,000 µg·m–3 and >200 µg·m–3 in asthmatics 6, 11. However, little is known about the impact of frequent, short-term exposure to high concentrations of NO2. In the present study of ice arenas, NO2 concentrations ranged from 29–1,015 µg·m–3 (mean 276 µg·m–3), and concentrations of the same magnitude of NO2 have been reported by others 6, 7. The wide range of concentrations could probably be explained by differences in ventilation systems, type and function of catalytic converter, size of the arena and activity on the ice.
The prevalence of "ever asthma" was 16% compared to 10.8% in a Swedish part of the ISAAC study investigating 13–14-yr-olds 12. Conversely, symptoms of asthma and rhinitis were not more frequent than in the ISAAC study. Exercise is an important provoking factor for asthma in individuals with bronchial hyperreactivity. Physically active children may have an increased perception or awareness of respiratory symptoms, which may explain the high prevalence of asthma in the present study. Sports are often recommended in asthmatic children as one of the cornerstones in asthma treatment. This may contribute to the high prevalence of asthma among athletic children also shown by other investigators 13. However, the increase of the asthma prevalence in the present study could also be due to a true increase of the asthma occurrence among children attending ice arenas. Recently, several studies have indicated a relationship between athletics and asthma. Thirty one per cent of Swedish elite cross-country skiers have exercise-induced asthma 14. In a Swiss study, it was demonstrated that ice hockey players had higher prevalence of asthma and bronchial hyperresponsiveness than floor ball players 15. An American investigation involving 121 elite ice skaters showed exercise-induced bronchoconstriction in 35% of the skaters 16. However, neither of the two latter studies presented objective measurements on air quality. It was suggested that exercising on ice at temperatures 5–10°C, compared to training at higher temperatures, could induce bronchial hyperresponsiveness.
Questionnaire-based information on prevalence is widely used in asthma epidemiology in combination with cross-sectional methodology. This design has disadvantages related to control of certain types of bias, such as recall bias. Conversely, the question on "physician diagnosed asthma" is shown to have very high specificity, near 100%, and a sensitivity of about 70% in a study with similar design and age group 17. However, a poor sensitivity has less effect on the estimation of OR than poor specificity of the health outcome assessment 18.
Selection bias could contribute to the lack of difference in symptom prevalence between propane arenas and electric arenas. The insurance file that was used to identify study subjects only registered children from the age of 10 when they become licensed players in Sweden. Consequently, children who stopped hockey or figure skating before that age were not included and some children may have experienced more discomfort in the propane arenas and quit or changed sports before the age of ten. The fact that children in electric arenas showed a tendency to report more atopy and parental atopy supports this hypothesis. Furthermore, it is possible that some children in the electric-arena group had regular activities in propane arenas during tournaments and matches, contributing to a smaller exposure contrast and difficulties in detecting exposure-related differences in health outcomes.
In conclusion, children with >3 yrs of frequent exposure to very high concentrations of nitrogen dioxide in ice arenas using propane-powered ice-resurfacing machines did not have a higher prevalence of asthma or rhinitis than children in ice arenas using electric resurfacing machines. However, children exposed to the highest concentrations of nitrogen dioxide had more respiratory symptoms, particularly nasal symptoms, than children exposed to lower concentrations. Furthermore, the overall prevalence of asthma appears high among children playing ice hockey.
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