The Effect of Outdoor Aeroallergens on Asthma Hospitalizations in Children in North-Western Tuscany, Italy
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Design and Area
2.2. Asthma-like Symptoms Admissions
2.3. Outdoor Aeroallergen Counts
2.4. Time-Varying Confounders
2.5. Statistical Analyses
3. Results
3.1. Characteristics of the Study Population
3.2. Outdoor Aeroallergen Effects
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Sestini, P.; De Sario, M.; Bugiani, M.; Bisanti, L.; Giannella, G.; Kaisermann, D.; Frasca, G.; Lombardi, E.; Petronio, M.G.; Dell’Orco, V.; et al. Gruppo Collaborativo SIDRIA-2. Frequency of asthma and allergies in Italian children and adolescents: Results from SIDRIA-2. Epidemiol. Prev. 2005, 29 (Suppl. S2), 24–31. [Google Scholar] [PubMed]
- Murray, C.S.; Poletti, G.; Kebadze, T.; Morris, J.; Woodcock, A.; Johnston, S.L.; Custovic, A. Study of modifiable risk factors for asthma exacerbations: Virus infection and allergen exposure increase the risk of asthma hospital admissions in children. Thorax 2006, 61, 376–382. [Google Scholar] [CrossRef] [Green Version]
- Dales, R.E.; Cakmak, S.; Judek, S.; Dann, T.; Coates, F.; Brook, J.R.; Burnett, R.T. Influence of outdoor aeroallergens on hospitalization for asthma in Canada. J. Allergy Clin. Immunol. 2004, 113, 303–306. [Google Scholar] [CrossRef]
- Osborne, N.J.; Alcock, I.; Wheeler, B.W.; Hajat, S.; Sarran, C.; Clewlow, Y.; McInnes, R.N.; Hemming, D.; White, M.; Vardoulakis, S.; et al. Pollen exposure and hospitalization due to asthma exacerbations: Daily time series in a European city. Int. J. Biometeorol. 2017, 61, 1837–1848. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Atkinson, R.W.; Strachan, D.P.; Anderson, H.R.; Hajat, S.; Emberlin, J. Temporal associations between daily counts of fungal spores and asthma exacerbations. Occup. Environ. Med. 2006, 63, 580–590. [Google Scholar] [CrossRef] [Green Version]
- Erbas, B.; Jazayeri, M.; Lambert, K.A.; Katelaris, C.H.; Prendergast, L.A.; Tham, R.; Parrodi, M.J.; Davies, J.; Newbigin, E.; Abramson, M.J.; et al. Outdoor pollen is a trigger of child and adolescent asthma emergency department presentations: A systematic review and meta-analysis. Allergy 2018, 73, 1632–1641. [Google Scholar] [CrossRef] [PubMed]
- Shrestha, S.K.; Lambert, K.A.; Erbas, B. Ambient pollen concentrations and asthma hospitalization in children and adolescents: A systematic review and meta-analysis. J. Asthma 2021, 58, 1155–1168. [Google Scholar] [CrossRef] [PubMed]
- Tham, R.; Katelaris, C.H.; Vicendese, D. The role of outdoor fungi on asthma hospital admissions in children and adolescents: A 5-year time stratified case-crossover analysis. Environ. Res. 2017, 154, 42–49. [Google Scholar] [CrossRef]
- Batra, M.; Vicendese, D.; Newbigin, E.; Lambert, K.A.; Tang, M.; Abramson, M.J.; Shyamali, C.; Dharmage, S.C.; Erbas, B. The association between outdoor allergens—Pollen, fungal spore season and high asthma admission days in children and adolescents. Int. J. Environ. Health Res. 2021. online ahead of print. [Google Scholar] [CrossRef]
- D’Amato, G.; Cecchi, L.; Bonini, S.; Nunes, C.; Annesi-Maesano, I.; Behrendt, H.; Liccardi, G.; Popov, T.; van Cauwenberge, P. Allergenic pollen and pollen allergy in Europe. Allergy 2007, 62, 976–990. [Google Scholar] [CrossRef]
- Tosca, M.A.; Ruffoni, S.; Canonica, G.W.; Ciprandi, G. Asthma exacerbation in children: Relationship among pollens, weather, and air pollution. Allergol. Immunopathol. 2014, 42, 362–368. [Google Scholar] [CrossRef]
- Bono, R.; Romanazzi, V.; Bellisario, V.; Tassinari, R.; Trucco, G.; Urbino, A.; Cassardo, C.; Siniscalco, C.; Marchetti, P.; Marcon, A. Air pollution, aeroallergens and admissions to pediatric emergency room for respiratory reasons in Turin, northwestern Italy. BMC Public Health 2016, 16, 722. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lawrence, M.C. The Relationship between Relative Humidity and the Dewpoint Temperature in Moist Air: A Simple Conversion and Applications. Bull. Am. Meteor. Soc. 2005, 86, 225–277. [Google Scholar] [CrossRef]
- O’Neill, M.S.; Zanobetti, A.; Schwartz, J. Modifiers of the Temperature and Mortality Association in Seven US Cities. Am. J. Epidemiol. 2003, 157, 1074–1082. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Maclure, M. The case-crossover design: A method for studying transient effects on the risk of acute events. Am. J. Epidemiol. 1991, 133, 144–153. [Google Scholar] [CrossRef] [PubMed]
- Carracedo-Martínez, E.; Taracido, M.; Tobias, A.; Saez, M.; Figueiras, A. Case-crossover analysis of air pollution health effects: A systematic review of methodology and application. Environ. Health Perspect. 2010, 118, 1173–1182. [Google Scholar] [CrossRef] [PubMed]
- Lachin, J.M. Sample size evaluation for a multiply matched case-control study using the score test from a conditional logistic (discrete Cox PH) regression model. Stat. Med. 2008, 27, 2509–2523. [Google Scholar] [CrossRef] [PubMed]
- Fasola, S.; Maio, S.; Baldacci, S.; La Grutta, S.; Ferrante, G.; Forastiere, F.; Stafoggia, M.; Gariazzo, C.; Silibello, C.; Carlino, G.; et al. Short-Term Effects of Air Pollution on Cardiovascular Hospitalizations in the Pisan Longitudinal Study. Int. J. Environ. Res. Public Health 2021, 18, 1164. [Google Scholar] [CrossRef] [PubMed]
- Schwartz, J. Is There Harvesting in the Association of Airborne Particles with Daily Deaths and Hospital Admissions? Epidemiology 2001, 12, 55–61. [Google Scholar] [CrossRef]
- Solimini, A.G.; Renzi, M. Association between Air Pollution and Emergency Room Visits for Atrial Fibrillation. Int. J. Environ. Res. Public Health 2017, 14, 661. [Google Scholar] [CrossRef]
- Erbas, B.; Akram, M.; Dharmage, S.C.; Tham, R.; Dennekamp, M.; Newbigin, E.; Taylor, P.; Tang, M.L.K.; Abramson, M.J. The role of seasonal grass pollen on childhood asthma emergency department presentations. Clin. Exp. Allergy 2012, 42, 799–805. [Google Scholar] [CrossRef]
- Marques Mejías, M.A.; Tomás Pérez, M.; Hernández, I.; López, I.; Quirce, S. Asthma Exacerbations in the Pediatric Emergency Department at a Tertiary Hospital Association with Environmental Factors. J. Investig. Allergol. Clin. Immunol. 2019, 29, 365–370. [Google Scholar] [CrossRef] [PubMed]
- Geller-Bernstein, C.; Portnoy, J.M. The Clinical Utility of Pollen Counts. Clin. Rev. Allergy Immunol. 2019, 57, 340–349. [Google Scholar] [CrossRef] [PubMed]
- Di Cicco, M.; D’Elios, S.; Peroni, D.G.; Comberiati, P. The role of atopy in asthma development and persistence. Curr. Opin. Allergy Clin. Immunol. 2020, 20, 131–137. [Google Scholar] [CrossRef] [PubMed]
- Kim, H.Y.; Shin, Y.H.; Han, M.Y. Determinants of sensitization to allergen in infants and young children. Korean J. Pediatr. 2014, 57, 205–210. [Google Scholar] [CrossRef] [PubMed]
- Lee, S.W.; Yon, D.K.; James, C.C.; Lee, S.; Koh, H.Y.; Sheen, Y.H.; Oh, J.W.; Han, M.Y.; Sugihara, G. Short-term effects of multiple outdoor environmental factors on risk of asthma exacerbations: Age-stratified time-series analysis. J. Allergy Clin. Immunol. 2019, 144, 1542–1550. [Google Scholar] [CrossRef] [Green Version]
- Huang, W.; Schinasi, L.H.; Kenyon, C.C.; Moore, K.; Melly, S.; Hubbard, R.A.; Zhao, Y.; Diez Roux, A.V.; Forrest, C.B.; Maltenfort, M.; et al. Effects of ambient air pollution on childhood asthma exacerbation in the Philadelphia metropolitan Region, 2011–2014. Environ. Res. 2021, 197, 110955. [Google Scholar] [CrossRef]
- Valero, A.; Justicia, J.L.; Antón, E.; Dordal, T.; Fernández-Parra, B.; Lluch, M.; Montoro, J.; Navarro, A.M. Epidemiology of allergic rhinitis caused by grass pollen or house-dust mites in Spain. Am. J. Rhinol. Allergy 2011, 25, e123–e128. [Google Scholar] [CrossRef]
- De Roos, A.J.; Kenyon, C.C.; Zhao, Y.; Moore, K.; Melly, S.; Hubbard, R.A.; Henrickson, S.E.; Forrest, C.B.; Diez Roux, A.V.; Maltenfort, M.; et al. Ambient daily pollen levels in association with asthma exacerbation among children in Philadelphia, Pennsylvania. Environ. Int. 2020, 145, 106138. [Google Scholar] [CrossRef]
- Gleason, J.A.; Bielory, L.; Fagliano, J.A. Associations between ozone, PM2.5, and four pollen types on emergency department pediatric asthma events during the warm season in New Jersey: A case-crossover study. Environ. Res. 2014, 132, 421–429. [Google Scholar] [CrossRef]
- Hoffmann, T.M.; Şahin, A.A.; Aggelidis, X.; Arasi, S.; Barbalace, A.; Bourgoin, A.; Bregu, B.; Brighetti, M.A.; Caeiro, E.; Caglayan Sozmen, S.; et al. “Whole” vs. “fragmented” approach to EAACI pollen season definitions: A multicenter study in six Southern European cities. Allergy 2020, 75, 1659–1671. [Google Scholar] [CrossRef] [Green Version]
- Tham, R.; Erbas, B.; Dharmage, S.C.; Tang, M.L.; Aldakheel, F.; Lodge, C.J.; Thomas, P.S.; Taylor, P.E.; Abramson, M.J.; Lowe, A.J. Outdoor fungal spores and acute respiratory effects in vulnerable individuals. Environ. Res. 2019, 178, 108675. [Google Scholar] [CrossRef] [PubMed]
- Shrestha, S.K.; Katelaris, C.; Dharmage, S.C.; Burton, P.; Vicendese, D.; Tham, R.; Abramson, M.J.; Erbas, B. High ambient levels of grass, weed and other pollen are associated with asthma admissions in children and adolescents: A large 5-year case-crossover study. Clin. Exp. Allergy 2018, 48, 1421–1428. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cakmak, S.; Dales, R.E.; Judek, S.; Coates, F. Does socio-demographic status influence the effect of pollens and molds on hospitalization for asthma? Results from a time-series study in 10 Canadian cities. Ann. Epidemiol. 2005, 15, 214–218. [Google Scholar] [CrossRef] [PubMed]
- Di Cicco, M.; Kantar, A.; Masini, B.; Nuzzi, G.; Ragazzo, V.; Peroni, D. Structural and functional development in airways throughout childhood: Children are not small adults. Pediatr. Pulmonol. 2021, 56, 240–251. [Google Scholar] [CrossRef]
- Cecchi, L.; D’Amato, G.; Ayres, J.G.; Galan, C.; Forastiere, F.; Forsberg, B.; Gerritsen, J.; Nunes, C.; Behrendt, H.; Akdis, C.; et al. Projections of the effects of climate change on allergic asthma: The contribution of aerobiology. Allergy 2010, 65, 1073–1081. [Google Scholar] [CrossRef]
- Ayres, J.G.; Forsberg, B.; Annesi-Maesano, I.; Dey, R.; Ebi, K.L.; Helms, P.J.; Medina-Ramón, M.; Windt, M.; Forastiere, F. Climate change and respiratory disease: European Respiratory Society position statement. Eur. Respir. J. 2009, 34, 295–302. [Google Scholar] [CrossRef] [Green Version]
- Di Cicco, M.E.; Ferrante, G.; Amato, D.; Capizzi, A.; De Pieri, C.; Ferraro, V.A.; Furno, M.; Tranchino, V.; La Grutta, S. Climate Change and Childhood Respiratory Health: A Call to Action for Paediatricians. Int. J. Environ. Res. Public Health 2020, 17, 5344. [Google Scholar] [CrossRef]
- Katelaris, C.H.; Beggs, P.J. Climate change: Allergens and allergic diseases. Intern. Med. J. 2018, 48, 129–134. [Google Scholar] [CrossRef] [Green Version]
- Wayne, P.; Foster, S.; Connolly, J.; Bazzaz, F.; Epstein, P. Production of allergenic pollen by ragweed (Ambrosia artemisiifolia L.) is increased in CO2-enriched atmospheres. Ann. Allergy Asthma Immunol. 2002, 88, 279–282. [Google Scholar] [CrossRef]
- Lake, I.R.; Jones, N.R.; Agnew, M.; Goodess, C.M.; Giorgi, F.; Hamaoui-Laguel, L.; Semenov, M.A.; Solmon, F.; Storkey, J.; Vautardet, R.; et al. Climate Change and Future Pollen Allergy in Europe. Environ. Health Perspect. 2017, 125, 385–391. [Google Scholar] [CrossRef]
- Solomon, G.I.; Hjelmroos-Koski, M.; Rotkin-Ellman, M.; Hammond, S.K. Airborne mold and endotoxin concentrations in New Orleans, Louisiana, after flooding, October through November 2005. Environ. Health Perspect. 2006, 114, 1381–1386. [Google Scholar] [CrossRef] [PubMed]
- Ariano, R.; Canonica, G.W.; Passalacqua, G. Possible role of climate changes in variations in pollen seasons and allergic sensitizations during 27 years. Ann. Allergy Asthma Immunol. 2010, 104, 215–222. [Google Scholar] [CrossRef] [PubMed]
- Negrini, A.C.; Negrini, S.; Giunta, V.; Quaglini, S.; Ciprandi, G. Thirty-year survey on airborne pollen concentrations in Genoa, Italy: Relationship with sensitizations, meteorological data, and air pollution. Am. J. Rhinol. Allergy 2011, 25, e232–e241. [Google Scholar] [CrossRef] [PubMed]
Study Population | Overall n = 85 (100%) | Age 0–4 Years n = 40 (47%) | Age 5–17 Years n = 45 (53%) | p-Value |
---|---|---|---|---|
Disease group (ICD-9 code) | <0.001 | |||
Acute bronchitis (466.0) | 30 (35) | 26 (65) | 4 (9) | |
Asthma attacks (493, 519.11) | 46 (54) | 9 (23) | 37 (82) | |
Acute respiratory failure (518.81) | 9 (11) | 5 (12) | 4 (9) | |
Gender | 1.000 | |||
Female | 36 (42) | 17 (43) | 19 (42) | |
Male | 49 (58) | 23 (57) | 26 (58) | |
Aeroallergen sensitization § | <0.001 | |||
No sensitization | 24 (29) | 23 (59) | 1 (2) | |
Indoor sensitization | 23 (28) | 9 (23) | 14 (33) | |
Outdoor sensitization | 3 (4) | 0 (0) | 3 (7) | |
Indoor and outdoor sensitization | 32 (39) | 7 (18) | 25 (58) | |
History of respiratory symptoms | <0.001 | |||
Asthma only | 7 (8) | 1 (3) | 6 (13) | |
Allergic rhinitis only | 28 (33) | 17 (42) | 11 (25) | |
Asthma and allergic rhinitis | 30 (35) | 2 (5) | 28 (62) | |
None | 20 (24) | 20 (50) | 0 (0) |
Outdoor Aeroallergens | Control Days (n = 170) | Case Days (n = 85) | p-Value |
---|---|---|---|
Alternaria, grains/m3 | 11.85 (16.12) | 13.90 (18.39) | 0.210 |
Ambrosia, grains/m3 | 0.09 (0.57) | 0.22 (1.43) | 0.257 |
Betula, grains/m3 | 0.19 (1.00) | 0.17 (0.89) | 0.846 |
Cupressus, grains/m3 | 7.79 (27.70) | 13.93 (80.10) | 0.226 |
Graminaceae, grains/m3 | 6.93 (18.90) | 4.97 (11.13) | 0.227 |
Olive, grains/m3 | 1.82 (8.88) | 3.67 (14.15) | 0.070 |
Pinaceae, grains/m3 | 11.79 (34.15) | 25.95 (96.68) | 0.043 |
Urticaceae, grains/m3 | 6.30 (8.76) | 6.76 (8.47) | 0.618 |
Total, grains/m3 | 46.77 (63.06) | 69.57 (131.31) | 0.017 |
Lag | Overall (n = 85) | Outdoor Sensitization (n = 35) | No Outdoor Sensitization (n = 47) | Females (n = 36) | Males (n = 49) | 0–4 Years (n = 40) | 5–17 Years (n = 45) |
---|---|---|---|---|---|---|---|
Lag 0 | 1.054 [1.011, 1.098] | 1.085 [1.004, 1.173] | 1.037 [0.986, 1.091] | 1.034 [0.980, 1.091] | 1.069 [1.009, 1.132] | 1.030 [0.961, 1.105] | 1.065 [1.007, 1.127] |
Lag 1 | 1.037 [1.008, 1.067] | 1.058 [1.003, 1.115] | 1.025 [0.989, 1.063] | 1.026 [0.989, 1.065] | 1.046 [1.006, 1.088] | 1.018 [0.971, 1.069] | 1.046 [1.007, 1.087] |
Lag 2 | 1.021 [1.003, 1.039] | 1.031 [1.001, 1.061] | 1.014 [0.990, 1.038] | 1.018 [0.992, 1.045] | 1.024 [1.001, 1.048] | 1.007 [0.977, 1.038] | 1.027 [1.004, 1.052] |
Lag 3 | 1.005 [0.991, 1.019] | 1.004 [0.986, 1.023] | 1.002 [0.981, 1.024] | 1.01 [0.983, 1.038] | 1.003 [0.987, 1.020] | 0.995 [0.970, 1.022] | 1.009 [0.991, 1.026] |
Lag 4 | 0.989 [0.968, 1.011] | 0.979 [0.945, 1.013] | 0.991 [0.961, 1.021] | 1.002 [0.963, 1.043] | 0.982 [0.956, 1.01] | 0.984 [0.945, 1.024] | 0.991 [0.964, 1.018] |
Lag 5 | 0.974 [0.941, 1.007] | 0.954 [0.899, 1.012] | 0.979 [0.937, 1.023] | 0.994 [0.939, 1.053] | 0.962 [0.920, 1.006] | 0.973 [0.915, 1.034] | 0.973 [0.931, 1.016] |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 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
Di Cicco, M.; Del Tufo, E.; Fasola, S.; Gracci, S.; Marchi, M.G.; Fibbi, L.; Cilluffo, G.; Ferrante, G.; Peroni, D.G.; La Grutta, S. The Effect of Outdoor Aeroallergens on Asthma Hospitalizations in Children in North-Western Tuscany, Italy. Int. J. Environ. Res. Public Health 2022, 19, 3586. https://doi.org/10.3390/ijerph19063586
Di Cicco M, Del Tufo E, Fasola S, Gracci S, Marchi MG, Fibbi L, Cilluffo G, Ferrante G, Peroni DG, La Grutta S. The Effect of Outdoor Aeroallergens on Asthma Hospitalizations in Children in North-Western Tuscany, Italy. International Journal of Environmental Research and Public Health. 2022; 19(6):3586. https://doi.org/10.3390/ijerph19063586
Chicago/Turabian StyleDi Cicco, Maria, Ester Del Tufo, Salvatore Fasola, Serena Gracci, Maria Giovanna Marchi, Luca Fibbi, Giovanna Cilluffo, Giuliana Ferrante, Diego G. Peroni, and Stefania La Grutta. 2022. "The Effect of Outdoor Aeroallergens on Asthma Hospitalizations in Children in North-Western Tuscany, Italy" International Journal of Environmental Research and Public Health 19, no. 6: 3586. https://doi.org/10.3390/ijerph19063586