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1 Asthma centre, Armand Trousseau Hospital, Paris, 2 SEPIA Consulting Firm, Melrand, and 3 National Institute of Health and Medical Research INSERM U408, Paris, France
CORRESPONDENCE: C. Ségala, SEPIA, 18 bis rue du Calvaire, 56310, Melrand, France. Fax: 33 297288110. E-mail: sepia@sepia-sante.com
Keywords: air pollution, asthma in children, generalised estimating equations, panel study
Received: April 19, 2001
Accepted May 2, 2002
This study was supported by Agence de l'Environnement et de la Maitrise de l'Energie (ADEME, grant n° 9693018), Ministère de l'Environnement and Institut Electricité Santé.
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Abstract |
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Eighty-two medically diagnosed asthmatic children were followed up for 3 months. Outcomes included the incidence and prevalence of asthma attacks, nocturnal cough, supplementary use of ß2-agonists, symptoms of airway irritation, and peak expiratory flow (PEF) value and its variability. The statistical methods controlled for the lack of independence between daily health outcomes, temporal trends and pollen and weather conditions.
Black smoke and nitrogen dioxide (NO2) were associated with increases in the occurrence of nocturnal cough and respiratory infections. Ozone (O3) was associated with an increase in the occurrence of asthma attacks and respiratory infections and with changes in lung function, as shown by an increase in PEF variability and a decrease in PEF. Statistically significant interactions were demonstrated between O3 and temperature and between O3 and pollen count for asthma attacks. O3 levels had a greater effect on additional bronchodilator use and on irritations of the eyes, nose and throat on days on which no steroids were used. Particulate matter was associated with eye irritation only.
This study showed that, although within international air quality standards, the prevailing levels of photo-oxidant and particulate pollution in spring and early summer had measurable short-term effects on children with mild-to-moderate asthma.
The short-term effects of air pollution in humans are predominantly assessed by means of time series studies. These recently reviewed 1 studies have shown broadly consistent associations between air pollutants and a number of related outcomes, such as total mortality, cardiorespiratory mortality and hospital admissions. To ensure that relationships observed are causal, it is necessary to check that studies with different designs show similar associations 2 and that there is coherence between a broad range of related health outcomes 3. As recently reviewed 4, 5, panel studies provide these advantages. The health effects are measured on an individual basis, whereas the exposure data are mostly based on aggregated data. These studies are often conducted on the most susceptible subgroups of the population, such as children and asthmatics. Previously, a panel study was conducted in Paris, France 6, in which the detrimental effect of moderately high levels of winter air pollution on the symptoms and lung function of asthmatic children was demonstrated. As attention is increasingly focused on photo-oxidant air pollution episodes, a new study was conducted with the aim of assessing the short-term effects of photo-oxidant and particulate pollution on the health of medically diagnosed asthmatic children during spring and early summer.
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Methods |
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12 h·day–1 in Greater Paris; and had parents able to complete a diary. Fourteen of the children enrolled did not participate from the start of the study. During the 3 months of follow-up, children for whom the diary was not kept for 4 consecutive weeks, despite telephone reminders (n=2), or who gave inaccurate responses (n=2) were excluded. Table 1
summarises the characteristics and medication of the 82 participating children.
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Air pollution, weather and pollen data measurements
Ambient air pollution was routinely measured at the stations of the monitoring network (AIRPARIF) in the Greater Paris area. Data was retained from the urban background monitoring sites, which were representative of ambient air pollution in the geographical area and are not directly exposed to local sources. Recorded air pollution data included values for black smoke (BS; suspended black particulates), suspended particles with an aerodynamic diameter <13 µm (PM), sulphur dioxide (SO2), nitrogen dioxide (NO2) and ozone (O3) concentrations. PM (measured by ß-radiometry at five stations), SO2 (measured by ultraviolet (UV) fluorescence in 11 stations), and NO2 (measured by chemiluminescence at 14 stations) levels were measured hourly and a mean value was calculated for each day. The 24-h mean levels of BS were determined by reflectometry (French standard method NF-X 43-005) at 22 stations. The 8-h mean of O3 concentrations was measured (UV photometric analysers) at six stations. An overall mean of the mean daily readings at all stations was calculated because a previous study 7 demonstrated temporal and geographical homogeneity between data collected at the various stations. Mean daily temperature and relative humidity were determined at the Paris weather station (Météo France). Data on total pollen counts were collected by the French surveillance system for pollen counts (The Pasteur Institute, Paris, France, and the Aerobiological Monitoring Network, Paris, France).
Figure 1 shows the 24-h pattern of mean levels of PM, BS, NO2 and O3 during the study period. Pollution concentrations were moderate, with no pronounced peak. There was a very strong correlation between levels of NO2 and BS, with weaker correlations observed between NO2 and PM levels, and between O3 levels and particulate matter levels. As expected, there was no correlation between NO2 and O3 levels. SO2 was not considered in subsequent analysis because it was present only at low levels. High temperature was associated with high levels of O3, whereas low humidity was associated with high concentrations of the four pollutants, especially O3 (tables 2 and 3).
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3 mm. Each participant was given a new peak flow meter (mini-Wright; Clement Clarke International Ltd, Edinburgh, UK) to measure peak expiratory flow (PEF). They were instructed how to measure PEF in a standing position. The subject's parents had to complete a diary. Patients were followed for 3 months, from April 1, 1996 to June 30, 1996. At the end of each day, the parents recorded the presence or absence of asthma attacks, upper or lower respiratory infections with fever (defined as body temperature of >38°C) and the number of inhaled ß2-agonist puffs. They also recorded the severity of nocturnal cough, wheeze and symptoms of irritation, on a three-point scale as follows: 0=none, 1=moderate, 2=severe. Children recorded the best PEF of three attempts, three times per day (morning, afternoon and evening). Parents were asked to note if the child had spent the day outside the study area, and all such days were excluded from the analysis.
Diaries were collected weekly. Parents who did not return diaries or who returned incorrectly completed diaries were contacted by telephone. At the end of the study, two assessors that were not involved in the study checked the consistency of the responses. PEF measurements were considered invalid if values were identical for 1 week. Suitable data was available for a mean of 80% of the subjects per day.
Data transformation
For symptoms, days were classified as positive or negative with no account taken of the severity of symptoms for positive days. An incident episode for a given symptom was defined as the presence of the symptom on a given day when the previous day had been symptom-free. A prevalent episode was defined as the presence of the symptom on a given day irrespective of whether or not that symptom was also present on the previous day. Additional bronchodilator use was coded as a yes/no variable: yes if the number of puffs used on a given day was greater than that for the previous day.
For PEF values, data for the first 7 days were excluded from the analysis, as this period was considered to be a learning period. To eliminate the effect of the large differences between subjects' absolute PEF, each PEF value was converted into a Z score by subtracting the mean PEF for that child and dividing the result by the sd of all PEF values for that child 8. Daily PEF variability was calculated as the amplitude % mean 9:
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Statistical methods
Incident and prevalent episodes of asthma attacks, nocturnal cough, wheeze, symptoms of irritation, respiratory infections and supplementary use of ß2-agonist, Z-transformed morning PEF and daily PEF variability were used as health outcomes.
The association between air pollutants and health outcomes was evaluated by regression analysis based on the generalised estimating equations (GEE) proposed by Liang and Zeger 10, 11. These models correct for the repeated measurements in response data. The standard error of the regression estimate is therefore adjusted for the fact that responses from any one subject are likely to be correlated. This method generates robust estimators regardless of the specifications of the covariance matrix, and as autocorrelation is included in the covariance, coefficients can be interpreted as usual. The models are marginal logistic models for binary outcomes and marginal linear models for PEF variables.
The analysis was conducted in stages. According to the fit of the model, the procedure first determined the following covariates of the regression models: time trends (included as linear and if necessary, quadratic and cubic terms of the number of days since the start of the study), day of the week, pollen count (same day) and meteorological variables (with the inclusion, in some cases, of a quadratic term for temperature). Various temperature and humidity lags were investigated (
6 days), and, in the final model, the meteorological variables with the lag showing the strongest association with health outcomes were included (mostly lag 0, 1 or 2).
Pollutant measures (day 0) and cumulative pollutant measures (0–2 mean and 0–4 mean) were then entered in turn into the model. The effect of each pollutant on health was estimated by entering it separately into the models. Possible interactions between temperature and humidity, temperature and O3, and pollen and O3 were also assessed. If a significant interaction was found (p<0.05), an interaction term was introduced into the models. Finally, multipollutant models were conducted in which particles and O3 levels or NO2 and O3 levels were correlated with the same health outcome in one-pollutant models. An analysis restricted to person-days on which no steroid was used (979 person-days) was also carried out.
For binary response data, results are expressed as odds ratios (OR) with 95% confidence intervals (CI) for an increase of 10 µg·m–3 in pollutant concentration.
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Results |
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. As expected in this well-treated asthmatic population, the incidence of asthma attacks was lower than the incidence of nocturnal cough, wheeze and symptoms of irritation. The mean duration of episodes was 2–3 days. At this time of year, respiratory infections were rare.
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(incident episodes) and table 6 (prevalent episodes). Wheeze, whether incident or prevalent, was not correlated with the levels of any type of pollutant (not shown). Incident episodes of nocturnal cough were correlated with 0–2 mean BS (p=0.05) and with NO2 concentration at lag 0 (p=0.007). Prevalent episodes of nocturnal cough were correlated with 0–2 mean BS (p=0.02). Incident asthma attacks were significantly correlated at lag 0 with O3 level (p=0.02), only if the model included significant interactions between O3 and pollen (p=0.002) and O3 and temperature (p=0.01).
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Association between pollutants and respiratory infections
Incident episodes of respiratory infections (table 5
) were correlated at lag 0 and 0–2 mean with BS (p=0.0003 and p=0.04, respectively) and NO2 levels (p=0.0002 and p=0.04, respectively). Prevalent episodes of respiratory infections (table 6) were correlated at lag 0 and 0–2 mean with BS (p=0.0005 and p=0.01, respectively) and at lag 0 with NO2 levels (p=0.0003). If a term was included for the significant interaction between O3 and temperature, incident episodes of respiratory infections were correlated with 0–2 and 0–4 means for O3 concentration (p=0.009 and p=0.02, respectively). Similar results were obtained for prevalent episodes of respiratory infections. As incident episodes of respiratory infections were correlated with levels of O3 together with BS or NO2, multipollutant models were generated. BS level was not significant (p=0.15) in the multipollutant model that included BS, O3 and an interaction term between O3 and temperature. O3 level was not significant (p=0.08) in the multipollutant model that included NO2, O3 and an interaction term between O3 and temperature. As respiratory infections may confound the relationship between pollutants and health outcomes in asthmatic patients, all the models were re-run with respiratory infection as an additional explanatory variable. This slightly decreased the ORs obtained, but did not affect the significance of the effects observed (not shown).
Association between pollutants and symptoms of irritation
In the total population, incident episodes of nose or throat irritation were not correlated with the levels of any of the pollutants. Only incident episodes of eye irritation were correlated with O3 concentration at lag 0 (p=0.02), if a significant term of interaction between O3 and temperature was introduced. Prevalent episodes of eye irritation were significantly correlated with PM levels: OR=1.18, 95% CI 1.01–1.39 at lag 0; OR=1.28, 95% CI 1.03–1.59 at 0–2 mean; and OR=1.42, 95% CI 1.12–1.80 at 0–4 mean. Borderline associations were found between prevalent episodes of eye and throat irritations and BS and NO2 levels (not shown).
If the analysis was restricted to days on which no steroids were used by the children (table 7), symptoms were more strongly related to O3 and PM levels. O3 concentration was associated with incident episodes of nose (0–2 mean and 0–4 mean, p=0.05) and throat irritations (0–2 mean, p=0.001) and with prevalent episodes of eye (mean 0–4, p=0.03) and nose irritations (lag 0, p=0.008; mean 0–2, p=0.009; mean 0–4, p=0.02). PM was associated with prevalent episodes of eye irritation (mean 0–4, p=0.04). The interactions between O3 and temperature or pollen were not significant. In a multipollutant model assessing the independent effects of O3 and PM on prevalent episodes of eye irritation (mean 0–4), the O3 parameter remained stable but not significant (p=0.10), whereas the PM parameter decreased and was not significant (p=0.19).
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Discussion |
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In a previous study 6, it was shown that moderately high levels of winter air pollution were associated with increases in the incidence and prevalence of asthma attacks and asthma-like symptoms in children with mild asthma and with changes in lung function, as shown by the decrease in PEF and increase in PEF variability. In the study, only 49% of the asthmatic children (classified as moderately asthmatic) received both inhaled steroids and inhaled ß2-agonists daily, and in this group only supplementary ß2-agonist use was strongly associated with air pollution. By the time this study was performed, 74% of children received both inhaled steroids and inhaled ß2-agonists daily and it was not possible to distinguish between subgroups of asthmatics according to treatment. Nevertheless, the effect of air pollution on asthmatic children was still detectable during the spring and summer. In well-treated asthmatics, weaker associations between pollutant levels and asthma attacks or asthma-like symptoms would be expected, because asthmatics with an efficient maintenance treatment are able to manage their symptoms with supplementary medication. Indeed, the association between O3 levels and supplementary use of ß2-agonists was found only on days on which no steroids were used. Pope et al. 12 also reported weaker associations, except for the use of supplementary asthma medication, in a sample of asthmatic patients than in a school-based sample.
Panel studies are a powerful method for assessing the short-term effects of air pollution on human health. They have some limitations, which were discussed in detail in a previous paper 6. To date, most panel studies on asthmatic children have been conducted in winter 8, 13–18, with few focusing on the effects of spring and summer air pollution. Two studies were conducted in Los Angeles, CA, USA. In the first 19, in which 83 African-American asthmatic children were studied during a 4-month summer period, particles with a 50% cut-off aerodynamic diameter of 10 µm (PM10) and O3 were associated with shortness of breath, but not coughing and wheezing. In the second study 20, which included 138 children, the occurrence of shortness of breath, cough and wheeze was associated with PM10, particles with a 50% cut-off aerodynamic diameter of 2.5 µm (PM2.5), NO2 and moulds, but not with O3 and pollen, and the use of extra asthma medication was associated to PM10 and O3. During summer asthma camps in Connecticut, USA, O3 and fine particles (sulphate and hydrogen ions) were found to be significantly correlated with asthma exacerbation, chest symptoms, medication use and decreases in lung function 21. In San Diego, CA, USA, asthma symptoms were found to be significantly associated with PM10 and O3, and in agreement with the results of this study, stronger relationships were found in the subgroup of patients with mild asthma who were not taking anti-inflammatory medication 22. In two other panel studies 23, 24 conducted in Mexico City, Mexico, where there are high levels of pollution, symptoms and decreases in PEF were associated with O3 and PM10 levels. In a study conducted in the Netherlands 25, BS was associated with a decrease in PEF, acute respiratory symptoms and medication use. Weaker associations were found for PM10 and O3 levels.
The present study shows that O3 has detrimental effects on the following health outcomes in asthmatic children: occurrence of asthma attacks, additional bronchodilatator use, changes in lung function (as shown by the decrease in PEF and increase in PEF variability), and symptoms of irritation of the eyes, nose and throat. These results are consistent with the "Evaluation des Risques de la Pollution Urbaine sur la Santé" (ERPURS) study, which is part of the Air Pollution on Health, a European Approach (APHEA) project, conducted in Paris. Positive associations were observed for increases in levels of pollutants in children 26: a 3–8% increase in hospital admissions for asthma was observed for a 50 µg·m–3 increase in particle concentrations and a 1–3% increase in hospital admissions was observed for a 50 µg·m–3 increase in O3 or NO2 levels. A 50 µg·m–1 increase in particle or NO2 concentration was associated with a 30% increase in the number of doctors' house calls for asthma 27. In a similar manner to the present results, the relationship between asthma and O3 concentrations was restricted to days on which the temperature was high (>20°). O3 and temperature have a synergistic effect on several outcomes: asthma attacks, morning PEF and eye irritation. Together with climate and pollutants, ambient aeroallergens also influence asthma 20, 28. In the present study, only pollen count was available, and O3 and pollen count had a synergistic effect on the risk of asthma attacks. Recent experimental studies have shown that O3 may interact with air suspended allergens by amplifying the response to the allergen 29, 30.
The principal local source contributing to ambient air pollution in the Paris area at this time of the year is automobile exhaust fumes 31. The increases in vehicle traffic and the percentage of diesel engines 32 have contributed to the increase, since 1985, in emissions of nitrogen oxides, fine particulate matter, volatile organic compounds and O3 during spring and summer. Nevertheless, during the study period, levels of pollutants were well within European Community and World Health Organization standards. During the study period, NO2 and BS levels were highly correlated and both can, at this time of year, be considered as indicators of air pollutants emitted by diesel engines. This study also suggests that in an urban environment in spring to early summer, BS is more important than PM as an air pollution indicator associated with two acute effects in asthmatic children, nocturnal cough and respiratory infections. Only eye irritation was related to PM. A number of recent studies have suggested that PM2.5 is more strongly associated with health outcomes than PM10 33–35. The stronger associations observed for BS than for PM are consistent with the results of other studies conducted in Paris and elsewhere in Europe 25. Two multipollutant models were created to study the independent effect of O3 and particles, and found that particles made no independent contribution to respiratory infections and eye irritation. This finding is consistent with some other studies 21, 24. In contrast, Ostro et al. 20 reported greater effects of exposure to PM10 than exposure to O3 on asthmatics.
In conclusion, this study shows that, although within international air quality standards, the prevailing levels of photo-oxidant and particulate pollution in spring and early summer had measurable short-term effects on children with mild-to-moderate asthma.
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: O3; 
: PM; 
: NO2.