Abstract
A thunderstorm is a risk factor for severe respiratory allergy or asthma attacks in patients suffering from pollen/spore allergy. This study aimed to investigate the changes in the spectrum and quantity of pollen and fungal spores in the air of Bratislava during summer storms as well as the impact of selected environmental parameters on these changes. Pollen/spore samples were collected using a Burkard volumetric aerospore trap during summer 2016. To identify those types of pollen/spores that may harm human health during the storm episodes, we analysed how the concentration of individual bioparticles in the air changed during pre-storm/storm/post-storm periods. The effect of environmental variables on the concentration of selected pollen/spore types was evaluated through Spearman’s correlation analysis. The results of our study suggest that thunderstorm-related respiratory allergy symptoms in the study area may be caused by (1) spores of Myxomycetes, the airborne concentration of which increases due to an increase in wind speed during the pre-storm period; (2) ruptured pollen and Diatripaceae spores, the concentration of which increases due to increase in precipitation and relative air humidity, respectively, during the storm period; and (3) spores of Fusarium and Leptosphaeria, the concentration of which increases due to increase in precipitation and air temperature, respectively, during the post-storm period.
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References
Adhikari, A., Reponen, T., Grinshpun, S. A., Martyzevicius, D., & LeMasters, G. (2006). Correlation of ambient inhalable bioaerosols with particulate matter and ozone: a two-year study. Environmental Pollution, 140, 16–28. https://doi.org/10.1016/j.envpol.2005.07.004.
Alharbi, E., & Abdullah, M. (2019). Asthma attack prediction based on weather factors. PEN, 7, 408–419. https://doi.org/10.21533/pen.v7i1.422.
Allit, U. (2000). Airborne fungal spores and the thunderstorm of 24 June 1994. Aerobiologia, 16, 397–262. https://doi.org/10.1023/A:1026503500730.
Anderson, W., Prescott, G. J., Packham, S., Millins, J., Brookes, M., & Seaton, A. (2001). Asthma admissions and thunderstorms: a study of pollen, fungal spores, rainfall, and ozone. QJM Int J Med, 94, 429–433. https://doi.org/10.1093/qjmed/94.8.429.
Bartková-Ščevková, J. (2003). The influence of temperature, relative humidity and rainfall on the occurrence of pollen allergens (Betula, Poaceae, Ambrosia artemisiifolia) in the atmosphere of Bratislava (Slovakia). International Journal of Biometeorology, 48, 1–5. https://doi.org/10.1007/s00484-003-0166-2.
Bartra, J., Mullol, J., Del Guvillo, A., Dávila, I., Ferrer, M., Jáuregui, I., Montoro, J., Sastre, J., & Valero, A. (2007). Air pollution and allergens. Investig Allergol Clin Immunol, 17, 3–8.
Bellomo, R., Holmes, P., Gigliotti, P., Treloar, A., Suphioglu, C., Singh, M. B., & Knox, B. (1992). Two consecutive thunderstorm associated epidemics of asthma in the city of Melbourne. The possible role of rye grass pollen. The Medical Journal of Australia, 156, 834–837. https://doi.org/10.5694/j.1326-5377.1992.tb136994.x.
Benaissa, F., Bendahmane, I., Bourfis, N., Aoulaiche, O., & Alkama, R. (2019). Bioindication of urban air polycyclic aromatic hydrocarbons using Petunia hybrida. Civil Engineering Journal, 5, 1305–1313. https://doi.org/10.28991/cej-2019-03091333.
Bowatte, G., Erbas, B., Lodge, C. J., Knibbs, L. D., Gurrin, L. C., Marks, G. B., Thomas, P. S., Johns, D. P., Giles, G. G., Hui, J., Dennekamp, M., Perret, J. L., Abramson, M. J., Walters, E. H., Matheson, M. C., & Dharmage, S. C. (2017). Traffic-related air pollution exposure over a 5-year period is associated with increased risk of asthma and poor lung function in middle age. The European Respiratory Journal, 50, 1602357. https://doi.org/10.1183/13993003.02357-2016.
British Aerobiology Federation (1995). Airborne pollen and spores. A guide to trapping and counting. National Pollen and Hay fever Bureau, Rotherham.
Burge, H. A., & Rogers, C. A. (2000). Outdoor allergens. Environmental Health Perspectives, 108, 653–659. https://doi.org/10.1289/ehp.00108s4653.
Cairncross, E. K., John, J., & Zunckel, M. (2007). A novel air pollution index based on the relative risk of daily mortality associated with short-term exposure to common air pollutants. Atmospheric Environment, 41, 8442–8454. https://doi.org/10.1016/j.atmosenv.2007.07.003.
Campbell-Hewson, G., Cope, A., Egleston, C. V., Sherriff, H. M., Robinson, S. M., & Allitt, U. (1994). Epidemic of asthma possibly associated with electrical storms. BMJ, 309, 1086–1087. https://doi.org/10.1136/bmj.309.6961.1086a.
Cao, J., Hongmei, X., Qun, X., Bingheng, C., & Haidong, K. (2012). Fine particulate matter constituents and cardiopulmonary mortality in a heavily polluted Chinese city. Environmental Health Perspectives, 120, 373–378. https://doi.org/10.1289/ehp.1103671.
Celenza, A., Fothergill, J., Kupek, E., & Shaw, R. J. (1996). Thunderstorm associated asthma: a detailed analysis of environmental factors. British Medical Journal, 312, 604–607. https://doi.org/10.1136/bmj.312.7031.604.
Corden, J.M., Stepalska, D. (2006). Alternaria and Didymella spore concentrations in Derby, UK and Cracow, Poland. Can these fungal spore concentrations have a role in thunderstorm asthma. 8th International Congress on Aerobiology, Neuchâtel, Switzerland, 2006. Abstracts, p. 102.
Dales, R. E., Cakmak, S., Judek, S., Dann, T., Coates, F., Brook, J. R., & Burnett, R. T. (2003). The role of fungal spores in thunderstorm asthma. Chest, 123, 743–750. https://doi.org/10.1378/chest.123.3.745.
D'Amato, G., Cecchi, L., Bonini, S., Nunes, C., Annesi-Maesano, I., Behrendt, H., Liccardi, G., Popov, T., & van Cauwenberge, P. (2007). Allergenic pollen and pollen allergy in Europe. Allergy, 62, 976–990. https://doi.org/10.1111/j.1398-9995.2007.01393.x.
D'Amato, G., Cecchi, L., & Liccardi, G. (2008). Thunderstorm-related asthma: not only grass pollen and spores. The Journal of Allergy and Clinical Immunology, 121, 537–538. https://doi.org/10.1016/j.jaci.2007.10.046.
D'Amato, G., Baena-Cagnani, C. E., Cecchi, L., Annesi-Maesano, I., Nunes, C., Ansotegui, I., D’Amato, M., Liccardi, G., Sofia, M., & Canonica, W. G. (2013). Climate change, air pollution and extreme events leading to increasing prevalence of allergic respiratory diseases. Multidiscip Respir Med, 8, 12. https://doi.org/10.1186/2049-6958-8-12.
D'Amato, G., Vitale, C., D'Amato, M., Cecchi, L., Liccardi, G., Molino, A., Vatrella, A., Sanduzzi, A., Maesano, C., & Annesi-Maesano, I. (2016). Thunderstorm-related asthma: what happens and why. Clinical and Experimental Allergy, 46, 390–396. https://doi.org/10.1111/cea.12709.
D'Amato, G., Annesi-Maesano, I., Vaghi, A., Cecchi, L., & D'Amato, M. (2018). How do storm affect asthma? Current Allergy and Asthma Reports, 18, 24. https://doi.org/10.1007/s11882-018-0775-9.
Díez Herrero, A., Sabariego Ruiz, S., Gutiérrez Bustillo, M., & Cervigón Morales, P. (2006). Study of airborne fungal spores in Madrid, Spain. Aerobiologia, 22, 135–142. https://doi.org/10.1007/s10453-006-9025-z.
Girgis, S. T., Marks, G. B., Downs, S. H., Kolbe, A., Car, G. N., & Paton, R. (2000). Thunderstorm-associated asthma in an inland town in south-eastern Australia. Who is at risk? The European Respiratory Journal, 16, 3–8. https://doi.org/10.1034/j.1399-3003.2000.16a02.x.
Glikson, M., Rutherford, S., Simpson, R. W., Mitchel, C. A., & Yago, A. (1995). Microscopic and submicron components of atmospheric particulate matter during high asthma periods in Brisbane, Queensland, Australia. Atmospheric Environment, 29, 459–562. https://doi.org/10.1016/1352-2310(94)00278-S.
Grinn-Gofroń, A., & Strzelczak, A. (2013). Changes in concentration of Alternaria and Cladosporium spores during summer storms. International Journal of Biometeorology, 57, 759–768. https://doi.org/10.1007/s00484-012-0604-0.
Grinn-Gofroń, A., Strzelczak, A., & Wolski, T. (2011). The relationships between air pollutants, meteorological parameters and concentration of airborne fungal spores. Environmental Pollution, 159, 602–608. https://doi.org/10.1016/j.envpol.2010.10.002.
Grote, M., Vrtala, S., Niederberger, V., Wiermann, R., Valenta, R., & Reichelt, R. (2001). Release of allergen-bearing cytoplasm from hydrated pollen: A mechanism common to a variety of grass (Poaceae) species revealed by electron microscopy. The Journal of Allergy and Clinical Immunology, 108, 109–115. https://doi.org/10.1067/mai.2001.116431.
Hew, M., Lee, J., Susanto, N. H., Prasad, S., Bardin, P. G., Barnes, S., et al. (2019). The 2016 Melbourne thunderstorm asthma epidemic: Risk factors for severe attacks requiring hospital admission. Allergy, 74, 122–130. https://doi.org/10.1111/all.13609.
Ho, H.-M., Rao, C. Y., Hsu, H.-H., Chiu, Y.-H., Liu, C.-M., & Chao, H. J. (2005). Characteristics and determinants of ambient fungal spores in Hualien, Taiwan. Atmospheric Environment, 39, 5839–5850. https://doi.org/10.1016/j.atmosenv.2005.06.034.
Kallajxhiu, N., Kapidani, G., Naqellari, P., Pupuleku, B., Turku, S., Dauti, A., & Jançe, A. (2018). An allergopalynologic comparative study of the Humulus lupulus’ pollen grains (Cannabaceae) in different habitats. Thalassia Salentina, 40, 75–82. https://doi.org/10.1285/i15910725v40sup2p75.
Kallawicha, K., Chen, Y. C., Chao, H. J., Shen, W. C., Chen, B. Y., Chuang, Y. C., & Guo, Y. L. (2017). Ambient fungal spore concentration in subtropical metropolis: Temporal distributions and meteorological determinants. Aerosol and Air Quality Research, 17, 2051–2063. https://doi.org/10.4209/aaqr.2016.10.0450.
Kasprzyk, I., Rzepowska, B., & Wasylów, M. (2004). Fungal spores in the atmosphere of Rzeszów (South-East Poland). Annals of Agricultural and Environmental Medicine, 11, 285–289.
Khreis, H., Kelly, C., Tate, J., Parslow, R., Lucas, K., & Nieuwenhuijsen, M. (2017). Exposure to traffic-related air pollution and risk of development of childhood asthma: a systematic review and meta-analysis. Environment International, 100, 1–31. https://doi.org/10.1016/j.envint.2016.11.012.
Künzli, N., Kaise, R., Medina, S., Studnicka, M., Chanel, O., Fillinger, P., et al. (2000). Public-health impact of outdoor and traffic-related air pollution: a European assessment. Lancet, 356, 795–801. https://doi.org/10.1016/S0140-6736(00)02653-2.
Lacey, M. E., West, J. S. (2006). The air spora. The manual for catching and identifying airborne biological particles. Dordrecht, the Netherlands: Springer-Verlag Gmbh. https://doi.org/10.1111/j.1365-3059.2007.01610.x.
Lewis, S. A., Corden, J. M., Forster, G. E., & Newlands, M. (2000). Combined effects of aerobiological pollutants, chemical pollutants and meteorological conditions on asthma admissions and A & E attendances in Derbyshire UK, 1993 − 96. Clinical and Experimental Allergy, 30, 1724–1732. https://doi.org/10.1046/j.1365-2222.2000.00947.x.
Lierl, M. B., & Hornung, R. W. (2003). Relationship of outdoor air quality to paediatric asthma exacerbations. Annals of Allergy, Asthma, and Immunology, 90, 28–33. https://doi.org/10.1016/s1081-1206(10)63610-1.
Makra, L., Puskás, J., Matyasovszky, I., Csépe, Z., Lelovics, E., Bálint, B., & Tusnády, G. (2015). Weather elements, chemical air pollutants and airborne pollen influencing asthma emergency room visits in Szeged, Hungary: performance of two objective weather classifications. International Journal of Biometeorology, 59, 1269–1289. https://doi.org/10.1007/s00484-014-0938-x.
Marks, G. B., & Bush, R. K. (2007). Itˈs blowing in the wind: New insights into thunderstorm-related asthma. The Journal of Allergy and Clinical Immunology, 120, 530–532. https://doi.org/10.1016/j.jaci.2007.07.012.
Marks, G. B., Colquhoun, J. R., Girgis, S. T., Koski, M. H., Treloar, A. B. A., Hansen, P., et al. (2001). Thunderstorm outflows preceding epidemics of asthma during spring and summer. Thorax, 56, 468–471. https://doi.org/10.1136/thorax.56.6.468.
Monn, C. (2001). Exposure assessment of air pollutants: a review on spatial heterogeneity and indoor/outdoor/personal exposure to suspended particulate matter, nitrogen dioxide and ozone. Atmospheric Environment, 35, 1–32. https://doi.org/10.1016/S1352-2310(00)00330-7.
Motesaddi, S., Hashempour, Y., & Nowrouz, P. (2017). Characterizing of air pollution in Tehran: Comparison of two air quality indices. Civil Engineering Journal, 3, 749–758. https://doi.org/10.21859/cej-030911.
Motta, A. C., Marliere, M., Peltre, G., Sterenberg, P., & Lacroix, G. (2006). Traffic-related air pollutants induce the release of allergen-containing cytoplasmic granules from grass pollen. International Archives of Allergy and Immunology, 139, 294–298. https://doi.org/10.1159/000091600.
Mulenga, D., & Siziya, S. (2019). Indoor air pollution related respiratory ill health, a sequel of biomass use. AciMedicine Journal, 1, 30–37. https://doi.org/10.1016/j.trstmh.2008.05.028.
Murray, V., Venables, K., Laing-Morton, T., Partridge, M., Thurston, J., & Williams, D. J. (1994). Epidemic of asthma possibly related to thunderstorms. British Medical Journal, 309, 131–132. https://doi.org/10.1136/bmj.309.6947.131c.
Nasser, S. M., & Pulimood, T. B. (2009). Allergens and thunderstorm asthma. Current Allergy and Asthma Reports, 9, 384–390. https://doi.org/10.1007/s11882-009-0056-8.
Packe, G. E., & Ayers, J. G. (1986). Aeroallergen skin sensitivity in patients with severe asthma during a thunderstorm. Lancet, 1, 850–851. https://doi.org/10.1016/s0140-6736(86)90954-2.
Packe, G. E., & Ayres, J. G. (1985). Asthma outbreak during a thunderstorm. Lancet, 2, 199–204. https://doi.org/10.1016/s0140-6736(85)91510-7.
Pavord, J. D., Beasley, F. R., Agusti, A., Anderson, G. P., Bel, E., & Brusselle, G. (2018). After asthma: redefining airways diseases. Lancet, 391, 350–400. https://doi.org/10.1016/S0140-6736(17)30879-6.
Peden, D. B. (2001). Air pollution in asthma: effect of pollutants on airway inflammation. Annals of Allergy, Asthma & Immunology, 87, 12–17. https://doi.org/10.1016/s1081-1206(10)62334-4.
Pulimood, T. B., Corden, J. M., Bryden, C., Sharples, L., & Nasser, S. M. (2007). Epidemic asthma and the role of the fungal mould Alternaria alternata. The Journal of Allergy and Clinical Immunology, 120, 610–617. https://doi.org/10.1016/j.jaci.2007.04.045.
Pyrri, I., & Kapsanaki-Gotsi, E. (2017). Functional relations of airborne fungi to meteorological and pollution factors in a Mediterranean urban environment. Fungal Ecology, 30, 48–54. https://doi.org/10.1016/j.funeco.2017.08.007.
Risse, U., Tomczok, J., Huss-Marp, J., Darsow, U., & Behrendt, H. (2000). Health-relevant interaction between airborne particulate matter and aeroallergens (pollen). Journal of Aerosol Science, 31, 27–28. https://doi.org/10.1016/S0021-8502(00)90033-8.
Rosas, I., McCartney, H. A., Payne, R. W., Calderon, C., Lacey, J., Chapela, R., et al. (1998). Analysis of the relationship between environmental factors (aeroallergens, air pollution and weather) and asthma emergency admissions to a hospital in Mexico City. Allergy, 53, 394–401. https://doi.org/10.1111/j.1398-9995.1998.tb03911.x.
Sarnat, J. A., & Holguin, F. (2007). Asthma and air quality. Current Opinion in Pulmonary Medicine, 13, 63–66. https://doi.org/10.1097/MCP.0b013e3280117d25.
Ščevková, J., Dušička, J., Mičieta, K., & Somorčík, J. (2015). Diurnal variation in airborne pollen concentration of six allergenic tree taxa and its relationship with meteorological parameters. Aerobiologia, 31, 457–468. https://doi.org/10.1007/s10453-015-9379-1.
Ščevková, J., Hrabovský, M., Kováč, J., & Rosa, S. (2019). Intradiurnal variation of predominant airborne fungal spore biopollutants in the Central European urban environment. Environmental Science and Pollution Research, 26, 34603–34612. https://doi.org/10.1007/s11356-019-06616-7.
Sousa, S. I. V., Martins, F. G., Pereira, M. C., Alvim-Ferraz, M. C. M., Ribeiro, H., Oliveira, M., & Abreu, I. (2008). Influence of atmospheric ozone, PM10 and meteorological factors on the concentration of airborne pollen and fungal spores. Atmospheric Environment, 42, 7452–7464. https://doi.org/10.1016/j.atmosenv.2008.06.004.
Suphioglu, C., Singh, M. B., Taylor, P., Bellomo, R., Holmes, P., Puy, R., & Knox, R. B. (1992). Mechanism of grass-pollen-induced asthma. The Lancet, 339, 569–572. https://doi.org/10.1016/0140-6736(92)90864-y.
Thien, F., Beggs, P. J., Csutoros, D., Darvall, J., Hew, M., Davies, J. M., Bardin, P. G., Bannister, T., Barnes, S., Bellomo, R., Byrne, T., Casamento, A., Conron, M., Cross, A., Crosswell, A., Douglass, J. A., Durie, M., Dyett, J., Ebert, E., Erbas, B., French, C., Gelbart, B., Gillman, A., Harun, N. S., Huete, A., Irving, L., Karalapillai, D., Ku, D., Lachapelle, P., Langton, D., Lee, J., Looker, C., MacIsaac, C., McCaffrey, J., McDonald, C. F., McGain, F., Newbigin, E., O'Hehir, R., Pilcher, D., Prasad, S., Rangamuwa, K., Ruane, L., Sarode, V., Silver, J. D., Southcott, A. M., Subramaniam, A., Suphioglu, C., Susanto, N. H., Sutherland, M. F., Taori, G., Taylor, P., Torre, P., Vetro, J., Wigmore, G., Young, A. C., & Guest, C. (2018). The Melbourne epidemic thunderstorm asthma event 2016: an investigation of environmental triggers, effect on health services, and patient risk factors. Lancet Planet Health, 2, 255–263. https://doi.org/10.1016/S2542-5196(18)30120-7.
Tiedemann, A. V., & Firsching, K. H. (2000). Interactive effects of elevated ozone and carbon dioxide on growth and yield of leaf rust-infected versus non-infected wheat. Environmental Pollution, 108, 357–363. https://doi.org/10.1016/s0269-7491(99)00214-6.
Venables, K. M., Allit, U., Collier, C. G., Emberlin, J., Greig, J. B., & Hardaker, P. J. (1997). Thunderstorm-related asthma the epidemic of 24/25 June 1994. Clinical and Experimental Allergy, 27, 725–736. https://doi.org/10.1046/j.1365-2222.1997.790893.x.
Zhang, Y., Peng, L., Kan, H., Xu, J., Chen, R., Liu, Y., & Wang, W. (2014). Effects of meteorological factors on daily hospital admissions for asthma in adults: a time-series analysis. PLoS One, 9, e102475. https://doi.org/10.1371/journal.pone.0102475.
Żukiewicz-Sobczak, W. (2013). The role of fungi in allergic diseases. Postep Derm Alergol, 30, 42–45. https://doi.org/10.5114/pdia.2013.33377.
Acknowledgments
The authors acknowledge both the Division of Meteorology and Climatology (Faculty of Mathematics, Physics and Informatics of Comenius University in Bratislava) for providing meteorological data for Bratislava and the Slovak Hydrometeorological Institute (SHMÚ) for providing air pollution data used in this paper.
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This study was supported by the Operation Program of Research and Innovation for the project, Advancing University Capacity and Competence in Research, Development and Innovation, ITMS2014+: 313021X329, co-financed by the European Regional Development Fund. The study was also supported by Grant Agency VEGA (Bratislava), Grant Nos. 2/0054/18 and 1/0434/21.
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Ščevková, J., Dušička, J., Tropeková, M. et al. Summer storms and their effects on the spectrum and quantity of airborne bioparticles in Bratislava, Central Europe. Environ Monit Assess 192, 537 (2020). https://doi.org/10.1007/s10661-020-08497-7
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DOI: https://doi.org/10.1007/s10661-020-08497-7