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Relationship Between Ambient Ozone and Exhaled Nitric Oxide in Children
To the Editor: Ozone, an oxidant of photochemical smog, is known to cause a variety of respiratory effects, including diminished lung function, exacerbation of respiratory symptoms, and inflammation of airways.1 To date, lung inflammation has been measured only invasively, by analysis of bronchoalveolar lavage fluid obtained from adults exposed to relatively high concentrations of ozone while exercising.2-3 We used exhaled nitric oxide4 to measure the relationship between ambient ozone levels and inflammation of airways.
Methods
After parents had given their written informed consent, we examined 72 children, aged 6.5 to 15 years, attending 1 of 6 summer camps in rural southern Belgium. All children were healthy and free of asthma. Ambient ozone concentrations were continuously monitored at each camp during the time of our study (Ozone Analyzer Model 427, Signal Instrument Company, Faringdon, England) and checked for accuracy with data from the nearest local monitoring stations, which also measured other gaseous and particulate air pollutants (Interregional Cell of the Environment, Brussels, Belgium). The average 1- and 8-hour ozone concentrations were computed as the means of all 5-minute ozone concentrations.
Children remained outdoors throughout the day, engaged in various recreational activities but not sports or running. Their lung function, measured as forced vital capacity (FVC) and forced expiratory volume in 1 second (FEV1) (Compact II, Vitalograph Ltd, Buckingham, England), and their levels of exhaled nitric oxide (NIOX online analyzer, Aerocrine AB, Solna, Sweden) were measured indoors in each camp, both in the morning (10-12 AM) and in the evening (6-8 PM). Statistical comparisons between morning and afternoon values at each site were computed with a t test for differences.
Results
The maximum 8-hour average ambient ozone concentrations ranged from 37 to 159 µg/m3. Maximum 1-hour average levels attained values of 48 to 221 µg/m3, with highest levels in the evening. Concentrations of other air pollutants (nitrous oxides, particulate matter) were low and stable, or even decreased during the studied days (maximum 8-hour average concentrations of <25 µg/m3 for nitric oxide, nitrogen dioxide, and sulfur dioxide; and concentrations of <30 µg/m3 for airborne particulate matter with aerodynamic diameters <2.5 µm and of <50 µg/m3 for particulate matter with diameters <10 µm).
While a small evening decrease in levels of exhaled nitric oxide was observed in children exposed to ozone concentrations less than 100 µg/m3, those exposed to the highest ozone concentrations demonstrated a marked increase of their evening levels (Figure 1). Stepwise multiple regression analysis revealed no significant interaction of age, sex, height, or body mass index on the relationship between ozone concentration and levels of exhaled nitric oxide. The increase in levels of exhaled nitric oxide was not associated with a statistically significant reduction of either FVC and FEV1 (paired t test: P = .67 and P = .16, respectively).
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Figure. Levels of Exhaled Nitric Oxide in Children Exposed to Ambient Ozone
Children were exposed to increasing concentrations of ozone during 6 different summer camps in rural southern Belgium. Error bars indicate SD. P values are from paired t tests.
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Comment
We found evidence of lower respiratory tract inflammation in children exposed to higher levels of ambient ozone. The increased level of exhaled nitric oxide was pronounced at the 2 sites with an 8-hour concentration of 135 µg/m3 or greater. These 2 sites had maximum 1-hour concentrations of 167 and 221 µg/m3, which are both greater than the current US National Ambient Air Quality Standard (8-hour ozone concentration of 157 µg/m3),5 as well as both the US and EU population information levels (1-hour ozone concentrations of 235 and 180 µg/m3, respectively5-6). An inflammatory response might be triggered by even slightly lower ozone levels as suggested by the marked increase in the levels of exhaled nitric oxide we observed above an 8-hour ozone concentration of 110 µg/m3, whereas the evening levels of exhaled nitric oxide actually were lower at sites with lower 8-hour levels of ozone (Figure 1).
It is not surprising that these effects were not accompanied by lung function decrements, given the relatively low ozone exposure compared with previous studies7 and the lack of correlation between the inflammatory and respiratory function responses induced by ozone.8 Although the ozone-induced airways inflammation is likely to be detrimental only upon repetitive and sustained exposures, our data indicate that short-term effects of ozone can occur at levels lower than those allowed by current air quality standards.
Funding/Support: This study was supported by the European Union (HELIOS project, QLKA-1308).
Marc Nickmilder, PhD;
Sylviane Carbonnelle, MD;
Claire de Burbure, MD;
Alfred Bernard, PhD
Unit of Toxicology
Catholic University of Louvain
Brussels, Belgium
1. Lippmann M. Ozone. In: Lippmann M, ed. Environmental Toxicants. 2nd ed. New York, NY: Wiley-Interscience; 2000:655-724.
2. Devlin RB, McDonnell WF, Mann R, et al. Exposure of humans to ambient levels of ozone for 6.6 hours causes cellular and biochemical changes in the lung. Am J Respir Cell Mol Biol. 1991;4:72-81.
3. Kinney PL, Nilsen DM, Lippmann M, et al. Biomarkers of lung inflammation in recreational joggers exposed to ozone. Am J Respir Crit Care Med. 1996;154:1430-1435.
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4. Lehtimaki L, Kankaanranta H, Saarelainen S, et al. Extended exhaled NO measurement differentiates between alveolar and bronchial inflammation. Am J Respir Crit Care Med. 2001;163:1557-1561.
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5. US Environmental Protection Agency National Ambient Air Quality Standards, 65 Federal Register. 38855-38896 (1997).
6. EU Directive 2002/3/EC of the European Parliament and of the Council of 12 February 2002 relating to ozone in ambient air. Off J L. 2002;67:14-30.
7. Kinney PL, Thurston GD, Raizenne M. The effects of ambient ozone on lung function in children: a reanalysis of six summer camp studies. Environ Health Perspect. 1996;104:170-174.
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8. Balmes JR, Chen LL, Scannell C, et al. Ozone-induced decrements in FEV1 and FVC do not correlate with measures of inflammation. Am J Respir Crit Care Med. 1996;153:904-909.
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Letters Section Editor: Stephen J. Lurie, MD, PhD, Senior Editor.
JAMA. 2003;290:2546-2547.
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