The Influence of Short-Term Weather Parameters and Air Pollution on Adolescent Airway Inflammation
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Population
2.2. Assessment of Lung Function
2.3. Assessment of Environmental Exposures
2.4. Statistical Analysis
2.5. Sensitivity Analysis
3. Results
3.1. Description of Participants and Exposures
3.2. The Main Effects of Weather Variables and Air Pollution on FeNO
3.3. Interactive Effects of RH and Air Pollution on FeNO
3.4. Effect Modification
3.5. Sensitivity Analyses
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Soriano, J.B.; Kendrick, P.J.; Paulson, K.R.; Gupta, V.; Abrams, E.M.; Adedoyin, R.A.; Adhikari, T.B.; Advani, S.M.; Agrawal, A.; Ahmadian, E.; et al. Prevalence and attributable health burden of chronic respiratory diseases, 1990–2017: A systematic analysis for the Global Burden of Disease Study 2017. Lancet Respir. Med. 2020, 8, 585–596. [Google Scholar] [CrossRef] [PubMed]
- Lim, C.C.; Hayes, R.B.; Ahn, J.; Shao, Y.; Silverman, D.T.; Jones, R.R.; Garcia, C.; Bell, M.L.; Thurston, G.D. Long-Term Exposure to Ozone and Cause-Specific Mortality Risk in the United States. Am. J. Respir. Crit. Care Med. 2019, 200, 1022–1031. [Google Scholar] [CrossRef] [PubMed]
- Turner, S.W.; Chang, A.B.; Yang, I.A. Clinical utility of exhaled nitric oxide fraction in the management of asthma and COPD. Breathe 2019, 15, 306–316. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Z.; Zhang, H.; Yang, L.; Chen, X.; Norback, D.; Zhang, X. Associations between outdoor air pollution, ambient temperature and fraction of exhaled nitric oxide (FeNO) in university students in northern China—A panel study. Environ. Res. 2022, 212 Pt C, 113379. [Google Scholar] [CrossRef]
- Kocot, K.; Barański, K.; Melaniuk-Wolny, E.; Zajusz-Zubek, E.; Kowalska, M. Acute FeNO and Blood Pressure Responses to Air Pollution Exposure in Young Adults during Physical Activity. Int. J. Environ. Res. Public Health 2020, 17, 9012. [Google Scholar] [CrossRef] [PubMed]
- Abramson, M.J.; Wigmann, C.; Altug, H.; Schikowski, T. Ambient air pollution is associated with airway inflammation in older women: A nested cross-sectional analysis. BMJ Open Respir Res. 2020, 7, e000549. [Google Scholar] [CrossRef] [PubMed]
- Kress, S.; Kilanowski, A.; Wigmann, C.; Zhao, Q.; Zhao, T.; Abramson, M.J.; Gappa, M.; Standl, M.; Unfried, K.; Schikowski, T. Airway inflammation in adolescents and elderly women: Chronic air pollution exposure and polygenic susceptibility. Sci. Total Environ. 2022, 841, 156655. [Google Scholar] [CrossRef]
- Berhane, K.; Zhang, Y.; Salam, M.T.; Eckel, S.P.; Linn, W.S.; Rappaport, E.B.; Bastain, T.M.; Lurmann, F.; Gilliland, F.D. Longitudinal effects of air pollution on exhaled nitric oxide: The Children’s Health Study. Occup. Environ. Med. 2014, 71, 507. [Google Scholar] [CrossRef]
- Zhang, Y.; Eckel, S.P.; Berhane, K.; Garcia, E.; Muchmore, P.; Molshatzki, N.B.-A.; Rappaport, E.B.; Linn, W.S.; Habre, R.; Gilliland, F.D. Long-term exposures to air pollutants affect FeNO in children: A longitudinal study. Eur. Respir. J. 2021, 58, 2100705. [Google Scholar] [CrossRef]
- Trivedi, M.; Denton, E. Asthma in Children and Adults-What Are the Differences and What Can They Tell us About Asthma? Front. Pediatr. 2019, 7, 256. [Google Scholar] [CrossRef]
- Heinrich, J.; Brüske, I.; Cramer, C.; Hoffmann, U.; Schnappinger, M.; Schaaf, B.; von Berg, A.; Berdel, D.; Krämer, U.; Lehmann, I.; et al. GINIplus and LISAplus—Design and selected results of two German birth cohorts about natural course of atopic diseases and their determinants. Allergol. Sel. 2017, 1, 85–95. [Google Scholar] [CrossRef]
- American Thoracic Society; European Respiratory Society. ATS/ERS recommendations for standardized procedures for the online and offline measurement of exhaled lower respiratory nitric oxide and nasal nitric oxide, 2005. Am. J. Respir. Crit. Care Med. 2005, 171, 912–930. [Google Scholar] [CrossRef] [PubMed]
- Minkos, A.; Dauert, U.; Feigenspan, S.; Kessenger, S. Air Quality 2016: Preliminary Evaluation; Umweltbundesamt [German Environment Agency], Ed.; Umweltbundesamt: Dessau-Roßlau, Germany, 2017; p. 24. [Google Scholar]
- Bollmeyer, C.; Keller, J.D.; Ohlwein, C.; Wahl, S.; Crewell, S.; Friederichs, P.; Hense, A.; Keune, J.; Kneifel, S.; Pscheidt, I.; et al. Towards a high-resolution regional reanalysis for the European CORDEX domain. Q. J. R. Meteorol. Soc. 2015, 141, 1–15. [Google Scholar] [CrossRef]
- Zhao, T.; Markevych, I.; Standl, M.; Schulte-Körne, G.; Schikowski, T.; Berdel, D.; Koletzko, S.; Bauer, C.-P.; von Berg, A.; Nowak, D.; et al. Ambient ozone exposure and depressive symptoms in adolescents: Results of the GINIplus and LISA birth cohorts. Environ. Res. 2019, 170, 73–81. [Google Scholar] [CrossRef] [PubMed]
- R Core Team. R: A Language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria, 2021. [Google Scholar]
- Beck, H.E.; Zimmermann, N.E.; McVicar, T.R.; Vergopolan, N.; Berg, A.; Wood, E.F. Present and future Köppen-Geiger climate classification maps at 1-km resolution. Sci. Data 2018, 5, 180214. [Google Scholar] [CrossRef]
- Pidwirny, M. Physical Geography Lab Manual: The Atmosphere and Biosphere: Our Planet Earth. 2021. Available online: https://pressbooks.bccampus.ca/physgeoglabmanual1/ (accessed on 20 June 2023).
- Gehring, U.; Gruzieva, O.; Agius, R.M.; Beelen, R.; Custovic, A.; Cyrys, J.; Eeftens, M.; Flexeder, C.; Fuertes, E.; Heinrich, J.; et al. Air Pollution Exposure and Lung Function in Children: The ESCAPE Project. Environ. Health Perspect. 2013, 121, 1357–1364. [Google Scholar] [CrossRef]
- Han, A.; Deng, S.; Yu, J.; Zhang, Y.; Jalaludin, B.; Huang, C. Asthma triggered by extreme temperatures: From epidemiological evidence to biological plausibility. Environ. Res. 2023, 216, 114489. [Google Scholar] [CrossRef]
- Steinbacher, M.; Pfleger, A.; Schwantzer, G.; Jauk, S.; Weinhandl, E.; Eber, E. Small airway function before and after cold dry air challenge in pediatric asthma patients during remission. Pediatr. Pulmonol. 2017, 52, 873–879. [Google Scholar] [CrossRef]
- Goodman, M.; Hays, S. Asthma and swimming: A meta-analysis. J. Asthma. 2008, 45, 639–647. [Google Scholar] [CrossRef]
- Yang, L.; Zhao, S.; Gao, S.; Zhang, H.; Arens, E.; Zhai, Y. Gender differences in metabolic rates and thermal comfort in sedentary young males and females at various temperatures. Energy Build. 2021, 251, 111360. [Google Scholar] [CrossRef]
- Sarlani, E.; Farooq, N.; Greenspan, J.D. Gender and laterality differences in thermosensation throughout the perceptible range. Pain 2003, 106, 9–18. [Google Scholar] [CrossRef] [PubMed]
- Xu, R.; Li, S.; Guo, S.; Zhao, Q.; Abramson, M.J.; Li, S.; Guo, Y. Environmental temperature and human epigenetic modifications: A systematic review. Environ. Pollut. 2020, 259, 113840. [Google Scholar] [CrossRef] [PubMed]
- Kubesch, N.J.; de Nazelle, A.; Westerdahl, D.; Martinez, D.; Carrasco-Turigas, G.; Bouso, L.; Guerra, S.; Nieuwenhuijsen, M.J. Respiratory and inflammatory responses to short-term exposure to traffic-related air pollution with and without moderate physical activity. Occup. Environ. Med. 2015, 72, 284–293. [Google Scholar] [CrossRef] [PubMed]
- Clifford, S.; Mazaheri, M.; Salimi, F.; Ezz, W.N.; Yeganeh, B.; Low-Choy, S.; Walker, K.; Mengersen, K.; Marks, G.B.; Morawska, L. Effects of exposure to ambient ultrafine particles on respiratory health and systemic inflammation in children. Environ. Int. 2018, 114, 167–180. [Google Scholar] [CrossRef]
Characteristic | Overall 1 | Munich 1 | Wesel 1 | p-Value 2 |
---|---|---|---|---|
Number of Participants | 2042 | 1191 | 851 | |
Age | 15.06 (0.29) | 15.09 (0.29) | 15.02 (0.28) | 0.049 |
Sex Female Male | 1050 (51%) 992 (49%) | 609 (51%) 582 (49%) | 441 (52%) 410 (48%) | 0.8 |
Height (cm) | 171.4 (8.30) | 170.8 (8.22) | 172.4 (8.32) | <0.001 |
Weight (Kg) | 61.74 (11.96) | 60.46 (11.10) | 63.53 (12.86) | <0.001 |
FeNO (ppb) | 23.1 (20.94) | 25.48 (22.60) | 19.77 (17.86) | <0.001 |
Respiratory condition Yes No NA | 643 (31.5%) 1397 (68.4%) 2 (0.1%) | 388 (32.58%) 801 (67.25%) 2 (0.17%) | 255 (29.96%) 596 (70.04%) 0 | 0.2 |
Maximal parental education Low (<10 years) Medium (=10 years) High (>10 years) NA | 118 (5.78%) 539 (26.40%) 1380 (67.58%) 5 (0.24%) | 46 (3.86%) 210 (17.63%) 932 (78.25%) 3 (0.25%) | 72 (8.46%) 329 (38.66%) 448 (52.64%) 2 (0.24%) | <0.001 |
Body Mass Index (Kg/m2) Low (<18.5) Normal (18.5–24.9) High (>25) | 414 (20.27%) 1430 (70.03%) 198 (9.70%) | 257 (21.58%) 839 (70.45%) 95 (7.98%) | 157 (18.45%) 591 (69.45%) 103 (12.10%) | 0.004 |
Characteristic | Overall 1 | Munich 1 | Wesel 1 | p-Value 2 |
---|---|---|---|---|
Season Warm Cold | 1315 (64%) 727 (36%) | 776 (65%) 415 (35%) | 539 (63%) 312 (37%) | 0.4 |
Relative Humidity (%) | 75.22 (10.60) | 75.03 (11.07) | 75.49 (9.90) | 0.047 |
Tmax (°C) | 16.43 (7.83) | 16.50 (8.24) | 16.34 (7.22) | 0.6 |
Tmin (°C) | 8.61 (6.08) | 8.36 (6.13) | 8.95 (6.00) | 0.058 |
Tmean (°C) | 12.36 (6.80) | 12.24 (7.00) | 12.53 (6.50) | 0.4 |
PM2.5 (µg/m3) | 11.09 (6.58) | 9.75 (6.34) | 12.96 (6.46) | <0.001 |
NO2 (µg/m3) | 13.17 (8.39) | 16.29 (8.79) | 8.79 (5.28) | <0.001 |
O3 (µg/m3) | 53.54 (19.76) | 49.96 (20.98) | 58.55 (16.68) | <0.001 |
Tmax | Tmin | Tmean | ||||
---|---|---|---|---|---|---|
Percentage Change (95% CI) * | p-Value 1,* | Percentage Change (95% CI) * | p-Value 1,* | Percentage Change (95% CI) * | p-Value 1,* | |
RH 2 | −0.01 (−0.02, 0.01) | 0.265 | −0.01 (−0.03, 0.00) | 0.074 | −0.01 (−0.02, 0.00) | 0.179 |
PM2.5 | 0.19 (−0.24, 0.63) | 0.382 | 0.20 (−0.23, 0.64) | 0.355 | 0.20 (−0.23, 0.63) | 0.367 |
Temperature | 0.29 (−0.28, 0.86) | 0.314 | 0.27 (−0.41, 0.94) | 0.439 | 0.32 (−0.31, 0.96) | 0.321 |
RH 2 | −0.01 (−0.03, 0.01) | 0.316 | −0.01 (−0.03, 0.00) | 0.144 | −0.01 (−0.03, 0.01) | 0.237 |
O3 | 0.01 (−0.18, 0.19) | 0.949 | 0.02 (−0.17, 0.20) | 0.849 | 0.01 (−0.18, 0.20) | 0.928 |
Temperature | 0.31 (−0.29, 0.91) | 0.308 | 0.25 (−0.45, 0.95) | 0.486 | 0.33 (−0.33, 1.00) | 0.328 |
RH 2 | −0.01 (−0.03, 0.01) | 0.199 | −0.01 (−0.03, −0.00) | 0.039 | −0.01 (−0.03, 0.00) | 0.122 |
NO2 | 0.31 (−0.29, 0.91) | 0.117 | 0.32 (−0.07, 0.71) | 0.107 | 0.32 (−0.07, 0.71) | 0.109 |
Temperature | 0.35 (−0.22, 0.92) | 0.225 | 0.35 (−0.33, 1.04) | 0.311 | 0.40 (−0.24, 1.04) | 0.222 |
Interaction Term 2,* | Percentage Change (95% CI) 2,* | p-Value 1,* | |
---|---|---|---|
Tmax * | RH: High PM2.5 | 0.02 (−0.02, 0.06) | 0.256 |
RH: Medium PM2.5 | 0.02 (−0.02, 0.05) | 0.388 | |
Tmin * | RH: High PM2.5 | 0.02 (−0.02, 0.06) | 0.256 |
RH: Medium PM2.5 | 0.02 (−0.02, 0.05) | 0.389 | |
Tmean * | RH: High PM2.5 | 0.02 (−0.02, 0.06) | 0.258 |
RH: Medium PM2.5 | 0.02 (−0.02, 0.05) | 0.389 |
Interaction Term 2,* | Percentage Change (95% CI) 2,* | p-Value 1,* | |
---|---|---|---|
Tmax * | RH: High O3 | −0.04 (−0.09, −0.00) | 0.042 |
RH: Medium O3 | −0.04 (−0.07, −0.00) | 0.040 | |
Tmin * | RH: High O3 | −0.04 (−0.09, −0.00) | 0.042 |
RH: Medium O3 | −0.04 (−0.08, −0.00) | 0.038 | |
Tmean * | RH: High O3 | −0.04 (−0.09, −0.00) | 0.043 |
RH: Medium O3 | −0.04 (−0.07, −0.00) | 0.040 |
Interaction Term 2,* | Percentage Change (95% CI) 2,* | p-Value 1,* | |
---|---|---|---|
Tmax * | RH: High NO2 | 0.05 (0.01, 0.08) | 0.007 |
RH: Medium NO2 | 0.03 (0.00, 0.07) | 0.050 | |
Tmin * | RH: High NO2 | 0.05 (0.01, 0.08) | 0.008 |
RH: Medium NO2 | 0.03 (0.00, 0.07) | 0.050 | |
Tmean * | RH: High NO2 | 0.05 (0.01, 0.08) | 0.008 |
RH: Medium NO2 | 0.03 (0.00, 0.07) | 0.050 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Areal, A.T.; Singh, N.; Zhao, Q.; Berdel, D.; Koletzko, S.; von Berg, A.; Gappa, M.; Heinrich, J.; Standl, M.; Abramson, M.J.; et al. The Influence of Short-Term Weather Parameters and Air Pollution on Adolescent Airway Inflammation. Int. J. Environ. Res. Public Health 2023, 20, 6827. https://doi.org/10.3390/ijerph20196827
Areal AT, Singh N, Zhao Q, Berdel D, Koletzko S, von Berg A, Gappa M, Heinrich J, Standl M, Abramson MJ, et al. The Influence of Short-Term Weather Parameters and Air Pollution on Adolescent Airway Inflammation. International Journal of Environmental Research and Public Health. 2023; 20(19):6827. https://doi.org/10.3390/ijerph20196827
Chicago/Turabian StyleAreal, Ashtyn Tracey, Nidhi Singh, Qi Zhao, Dietrich Berdel, Sibylle Koletzko, Andrea von Berg, Monika Gappa, Joachim Heinrich, Marie Standl, Michael J. Abramson, and et al. 2023. "The Influence of Short-Term Weather Parameters and Air Pollution on Adolescent Airway Inflammation" International Journal of Environmental Research and Public Health 20, no. 19: 6827. https://doi.org/10.3390/ijerph20196827
APA StyleAreal, A. T., Singh, N., Zhao, Q., Berdel, D., Koletzko, S., von Berg, A., Gappa, M., Heinrich, J., Standl, M., Abramson, M. J., & Schikowski, T. (2023). The Influence of Short-Term Weather Parameters and Air Pollution on Adolescent Airway Inflammation. International Journal of Environmental Research and Public Health, 20(19), 6827. https://doi.org/10.3390/ijerph20196827