Abstract
Hirst-type sampler (HTS) is the standard equipment for pollen sampling while cascade impactors are commonly used for particulate matter (PM) samplings. In this work, we investigated the feasibility of using such devices to reliably assess the atmospheric PM adhesion onto pollen grains (PGs). Birch PGs were deposited on sampling substrates and then exposed to ambient PM in each type of sampling device operating simultaneously. In the HTS, the surface of PGs was significantly polluted with PM during sampling (93.5% of polluted PGs with on average 4 particles per PG with a mean diameter of 2.2 µm). A modified entrance slit was tested and proved to significantly reduce the PM sampling artifact (28% of polluted PGs), although not completely canceling it. In contrast, in the PM10 impactor, all PGs remained free from particulate pollutants. We concluded that the PM pollution of PGs reported in previous studies using a HTS may be overestimated. While PG samplings using a HTS might provide insights into the co-exposure to allergenic pollen and other ambient PM, a size-selective aerosol sampler proves to be more appropriate for a reliable assessment of the extent of PM pollution of airborne pollen in order to give a realistic depiction of the physical and chemical state of ambient PGs that could be inhaled.
Similar content being viewed by others
References
Ackaert, C., Kofler, S., Horejs-Hoeck, J., Zulehner, N., Asam, C., von Grafenstein, S., et al. (2014). The impact of nitration on the structure and immunogenicity of the major birch pollen allergen bet v 1.0101. PLoS ONE, 9(8), e104520. https://doi.org/10.1371/journal.pone.0104520.
Ali, Z., Thomas, C. L. P., & Alder, J. F. (1989). denuder tubes for sampling of Gaseous species. A Review Analyst, 114(7), 759–769. https://doi.org/10.1039/AN9891400759.
ANSES. (2014). Etat des connaissances sur l’impact sanitaire lié à l’exposition de la population générale aux pollens présents dans l’air ambiant. Anses.
Beck, I., Jochner, S., Gilles, S., McIntyre, M., Buters, J. T., Schmidt-Weber, C., et al. (2013). High environmental ozone levels lead to enhanced allergenicity of birch pollen. PLoS ONE, 8(11), e80147.
Behrendt, H., Becker, W. M., Friedrichs, K. H., Darsow, U., & Tomingas, R. (1992). Interaction between aeroallergens and airborne particulate matter. International Archives of Allergy and Immunology, 99(2–4), 425–428.
Bradley, D. E. (1958). The study of pollen grain surfaces in the electron microscope. New Phytologist, 57(2), 226–229. https://doi.org/10.1111/j.1469-8137.1958.tb05308.x.
Bryce, M., Drews, O., Schenk, M., Menzel, A., Estrella, N., Weichenmeier, I., et al. (2010). Impact of urbanization on the proteome of birch pollen and its chemotactic activity on human granulocytes. International Archives of Allergy and Immunology, 151(1), 46–55.
Burte, E., Leynaert, B., Marcon, A., Bousquet, J., Benmerad, M., Bono, R., et al. (2020). Long-term air pollution exposure is associated with increased severity of rhinitis in 2 European cohorts. Journal of Allergy and Clinical Immunology. https://doi.org/10.1016/j.jaci.2019.11.040.
Buters, J. T. M., Antunes, C., Galveias, A., Bergmann, K. C., Thibaudon, M., Galán, C., et al. (2018). Pollen and spore monitoring in the world. Clinical and Translational Allergy, 8, 9. https://doi.org/10.1186/s13601-018-0197-8.
Cariñanos, P., Galán, C., Alcázar, P., & Dominguez, E. (1998). Spectrophotometric analysis as a complementary technique to aerobiology in the study of solid particles in the air. Aerobiologia, 14(2), 249–253. https://doi.org/10.1007/BF02694214.
Cariñanos, P., Galán, C., Alcázar, P., & Dominguez, E. (2000). Meteorological phenomena affecting the presence of solid particles suspended in the air during winter. International Journal of Biometeorology, 44(1), 6–10. https://doi.org/10.1007/s004840050132.
Carvalho, T. C., Peters, J. I., & Williams, R. O. (2011). Influence of particle size on regional lung deposition—what evidence is there? International Journal of Pharmaceutics, 406(1), 1–10. https://doi.org/10.1016/j.ijpharm.2010.12.040.
Chehregani, A., & Kouhkan, F. (2008). Diesel Exhaust particles and allergenicity of pollen grains of Lilium martagon. Ecotoxicology and Environmental Safety, 69(3), 568–573.
Choël, M., Deboudt, K., & Flament, P. (2010). Development of time-resolved description of aerosol properties at the particle scale during an episode of industrial pollution plume. Water Air and Soil Pollution, 209(1), 93–107. https://doi.org/10.1007/s11270-009-0183-9.
Cuinica, L. G., Abreu, I., Gomes, C. R., & Esteves da Silva, J. C. G. (2013). Exposure of Betula pendula Roth pollen to atmospheric pollutants CO, O3 and SO2. Grana, 52(4), 299–304. https://doi.org/10.1080/00173134.2013.830145.
Cuinica, L. G., Abreu, I., & Esteves da Silva, J. (2014). Effect of air pollutant NO2 on Betula pendula, Ostrya carpinifolia and Carpinus betulus pollen fertility and human allergenicity. Environmental Pollution, 186, 50–55. https://doi.org/10.1016/j.envpol.2013.12.001.
Cuinica, L. G., Cruz, A., Abreu, I., & da Silva, J. (2015). Effects of atmospheric pollutants (CO, O3, SO2) on the allergenicity of Betula pendula, Ostrya carpinifolia, and Carpinus betulus pollen. International Journal of Environmental Health Research, 25(3), 312–321. https://doi.org/10.1080/09603123.2014.938031.
D’amato, G., (2000). Urban air pollution and plant-derived respiratory allergy. Clinical and Experimental Allergy, 30(628), 636.
D’Amato, G. (2002). Environmental urban factors (air pollution and allergens) and the rising trends in allergic respiratory diseases. Allergy, 57(s72), 30–33.
Darbah, J., Kubiske, M. E., Nelson, N., & Vaapavuori, E. (2007). Impacts of elevated atmospheric CO2 and O3 on paper birch (Betula papyrifera): Reproductive Fitness. The Scientific World Journal, 7, 240–246.
Davies, R. J., Rusznak, C., & Devalia, J. L. (1998). Why is allergy increasing?—environmental factors. Clinical and Experimental Allergy, 28(S6), 8–14. https://doi.org/10.1046/j.1365-2222.1998.0280s6008.x.
Domínguez-Vilches, E., Cariñanos, P., Galán, C., Pasadas, F. G., García-Pantaleón, F. I., & de la Torre, F. V. (1995). Airborne pollen concentrations, solid particle content in the air and allergy symptoms in Córdoba (Spain). Aerobiologia, 11(2), 129–135. https://doi.org/10.1007/BF02738278.
Duque, L., Guimarães, F., Ribeiro, H., Sousa, R., & Abreu, I. (2012). Airborne Platanus pollen analysis by EPMA. Microscopy and Microanalysis, 18(S5), 39–40.
Duque, L., Guimarães, F., Ribeiro, H., Sousa, R., & Abreu, I. (2013). Elemental characterization of the airborne pollen surface using electron probe microanalysis (EPMA). Atmospheric Environment, 75, 296–302.
Erler, A., Hawranek, T., Krückemeier, L., Asam, C., Egger, M., Ferreira, F., et al. (2011). Proteomic profiling of birch (Betula verrucosa) pollen extracts from different origins. Proteomics, 11(8), 1486–1498. https://doi.org/10.1002/pmic.201000624.
Franze, T., Weller, M. G., Niessner, R., & Poschl, U. (2005). Protein nitration by polluted air. Environmental Science and Technology, 39(6), 1673–1678. https://doi.org/10.1021/es0488737.
Fruhstorfer, P., & Niessner, R. (1994). Identification and classification of airborne soot particles using an automated SEM/EDX. Microchimica Acta, 113(3), 239–250. https://doi.org/10.1007/BF01243614.
Galán, C., Smith, M., Thibaudon, M., Frenguelli, G., Oteros, J., Gehrig, R., et al. (2014). Pollen monitoring: Minimum requirements and reproducibility of analysis. Aerobiologia, 30(4), 385–395. https://doi.org/10.1007/s10453-014-9335-5.
Gong, Z., Pan, Y.-L., Videen, G., & Wang, C. (2019). Chemical reactions of single optically trapped bioaerosols in a controlled environment. Aerosol Science and Technology, 53(8), 853–859. https://doi.org/10.1080/02786826.2019.1621984.
Grewling, Ł., Bogawski, P., Kryza, M., Magyar, D., Sikoparija, B., Skjoth, C. A., et al. (2019a). Concomitant occurrence of anthropogenic air pollutants, mineral dust and fungal spores during long-distance transport of ragweed pollen. Environmental Pollution. https://doi.org/10.1016/j.envpol.2019.07.116.
Grewling, Ł., Frątczak, A., Kostecki, Ł., Nowak, M., Szymańska, A., & Bogawski, P. (2019b). Biological and chemical air pollutants in an urban area of central Europe: Co-exposure assessment. Aerosol and Air Quality Research. https://doi.org/10.4209/aaqr.2018.10.0365.
Gruijthuijsen, Y. K., Grieshuber, I., Söcklinger, A., Tischler, U., Fehrenbach, T., Weller, M. G., et al. (2006). Nitration enhances the allergenic potential of proteins. International Archives of Allergy and Immunology, 141(3), 265–275.
Guedes, A., Ribeiro, N., Ribeiro, H., Oliveira, M., Noronha, F., & Abreu, I. (2009). Comparison between urban and rural pollen of Chenopodium alba and characterization of adhered pollutant aerosol particles. Journal of Aerosol Science, 40(1), 81–86. https://doi.org/10.1016/j.jaerosci.2008.07.012.
Heinrich, J. (2019). Air pollutants and primary allergy prevention. Allergo Journal International, 28(1), 5–15. https://doi.org/10.1007/s40629-018-0078-7.
Helander, M. L., Savolainen, J., & Ahlholm, J. (1997). Effects of air pollution and other environmental factors on birch pollen allergens. Allergy, 52(12), 1207–1214.
Iwano, M., Wada, M., Morita, Y., Shiba, H., Takayama, S., & Isogai, A. (1999). X-ray microanalysis of papillar cells and pollen grains in the pollination process in Brassica using a variable-pressure scanning electron microscope. Journal of Electron Microscopy, 48(6), 909–917. https://doi.org/10.1093/oxfordjournals.jmicro.a023765.
Karle, A. C., Oostingh, G. J., Mutschlechner, S., Ferreira, F., Lackner, P., Bohle, B., et al. (2012). Nitration of the pollen allergen bet v 1.0101 enhances the presentation of bet v 1-derived peptides by HLA-DR on human dendritic cells. PLoS ONE, 7(2), e31483.
Khattab, A., & Levetin, E. (2008). Preliminary studies on the effect of the Burkard alternate orifice on airborne fungal spore concentrations. Aerobiologia, 24(3), 165–171. https://doi.org/10.1007/s10453-008-9096-0.
Knox, R. B., Suphioglu, C., Taylor, P., Desai, R., Watson, H. C., Peng, J. L., et al. (1997). Major grass pollen allergen Lol p 1 binds to diesel exhaust particles: implications for asthma and air pollution. Clinical and Experimental Allergy, 27(3), 246–251. https://doi.org/10.1111/j.1365-2222.1997.tb00702.x.
Kozlov, M. V., & Zvereva, E. L. (2004). Reproduction of mountain birch along a strong pollution gradient near Monchegorsk, Northwestern Russia. Environmental Pollution, 132, 443–451.
Leuschner, R. M., & Boehm, G. (1981). Pollen and inorganic particles in the air of climatically very different places in switzerland. Grana, 20(3), 161–167. https://doi.org/10.1080/00173138109427659.
Levetin, E. (2004). Methods for aeroallergen sampling. Current Allergy and Asthma Reports, 4(5), 376–383. https://doi.org/10.1007/s11882-004-0088-z.
Li, Z., Xu, X., Thompson, L. A., Gross, H. E., Shenkman, E. A., DeWalt, D. A., et al. (2019). Longitudinal effect of ambient air pollution and pollen exposure on asthma control: The PROMIS® pediatric asthma study. Academic Pediatrics. https://doi.org/10.1016/j.acap.2019.03.010.
Mahowald, N., Albani, S., Kok, J. F., Engelstaeder, S., Scanza, R., Ward, D. S., et al. (2014). The size distribution of desert dust aerosols and its impact on the earth system. Aeolian Research, 15, 53–71. https://doi.org/10.1016/j.aeolia.2013.09.002.
Majd, A., Chehregani, A., Moin, M., Gholami, M., Kohno, S., Nabe, T., et al. (2004). The effects of air pollution on structures, proteins and allergenicity of pollen grains. Aerobiologia, 20(2), 111–118.
Marple, V. A. (2004). History of impactors—The first 110 years. Aerosol Science and Technology, 38(3), 247–292. https://doi.org/10.1080/02786820490424347.
Marple, V. A., & Liu, B. Y. H. (1974). Characteristics of laminar jet impactors. Environmental Science and Technology, 8(7), 648–654. https://doi.org/10.1021/es60092a003.
Mazzarella, G., Esposito, V., Bianco, A., Ferraraccio, F., Prati, M. V., Lucariello, A., et al. (2012). Inflammatory effects on human lung epithelial cells after exposure to diesel exhaust micron sub particles (PM1.0) and pollen allergens. Environmental Pollution, 161, 64–69.
Mogo, S., Cachorro, V. E., & de Frutos, A. M. (2005). Morphological, chemical and optical absorbing characterization of aerosols in the urban atmosphere of valladolid. Atmospheric Chemistry and Physics, 5(10), 2739–2748. https://doi.org/10.5194/acp-5-2739-2005.
Mullins, J., & Emberlin, J. (1997). Sampling pollens. Journal of Aerosol Science, 28(3), 365–370. https://doi.org/10.1016/S0021-8502(96)00439-9.
Namork, E., Johansen, B. V., & Løvik, M. (2006). Detection of allergens adsorbed to ambient air particles collected in four European cities. Toxicology Letters, 165(1), 71–78.
Orellano, P., Quaranta, N., Reynoso, J., Balbi, B., & Vasquez, J. (2017). Effect of outdoor air pollution on asthma exacerbations in children and adults: Systematic review and multilevel meta-analysis. PLoS ONE, 12(3), e0174050. https://doi.org/10.1371/journal.pone.0174050.
Oteros, J., Buters, J., Laven, G., Röseler, S., Wachter, R., Schmidt-Weber, C., et al. (2016). Errors in determining the flow rate of hirst-type pollen traps. Aerobiologia. https://doi.org/10.1007/s10453-016-9467-x.
Pitz, M., Cyrys, J., Karg, E., Wiedensohler, A., Wichmann, H. E., & Heinrich, J. (2003). Variability of apparent particle density of an urban aerosol. Environmental Science and Technology, 37(19), 4336–4342. https://doi.org/10.1021/es034322p.
Reinmuth-Selzle, K., Ackaert, C., Kampf, C. J., Samonig, M., Shiraiwa, M., Kofler, S., et al. (2014). Nitration of the birch pollen allergen bet v 1.0101: Efficiency and site-selectivity of liquid and gaseous nitrating agents. Journal of Proteome Research, 13(3), 1570–1577. https://doi.org/10.1021/pr401078h.
Ribeiro, H., Guimarães, F., Duque, L., Noronha, F., & Abreu, I. (2015). Characterisation of particulate matter on airborne pollen grains. Environmental Pollution, 206, 7–16. https://doi.org/10.1016/j.envpol.2015.06.015.
Riediker, M., Koller, T., & Monn, C. (2000). Determination of birch pollen allergens in different aerosol sizes. Aerobiologia, 16(2), 251–254.
Ruggiero, F., & Bedini, G. (2018). Systematic and morphologic survey of orbicules in allergenic angiosperms. Aerobiologia, 34, 1–18.
Schäppi, G. F., Monn, C., Wüthrich, B., & Wanner, H. U. (1996). Analysis of allergens in ambient aerosols: comparison of areas subjected to different levels of air pollution. Aerobiologia, 12(1), 185–190.
Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., et al. (2012). Fiji: An open-source platform for biological-image analysis. Nature Methods, 9(7), 676–682. https://doi.org/10.1038/nmeth.2019.
Seinfeld, J. H., & Pandis, S. N. (2016). Atmospheric chemistry and physics: from air pollution to climate change. New Jersey: Wiley.
Sénéchal, H., Visez, N., Charpin, D., Shahali, Y., Peltre, G., Bioley, J.-P., et al. (2015). A review of the effects of major atmospheric pollutants on pollen grains, pollen content and allergenicity. The Scientific World Journal, ID 940243.
Sofiev, M., Siljamo, P., Ranta, H., & Rantio-Lehtimäki, A. (2006). Towards numerical forecasting of long-range air transport of birch pollen: theoretical considerations and a feasibility study. International Journal of Biometeorology, 50(6), 392–402. https://doi.org/10.1007/s00484-006-0027-x.
Visez, N., Ivanovsky, A., Roose, A., Gosselin, S., Sénéchal, H., Poncet, P., et al. (2020). Atmospheric particulate matter adhesion onto pollen: A review. Aerobiologia, 36(1), 49–62. https://doi.org/10.1007/s10453-019-09616-9.
Wittmaack, K. (2004). Characterization of carbon nanoparticles in ambient aerosols by scanning electron microscopy and model calculations. Journal of the Air and Waste Management Association, 54(9), 1091–1098. https://doi.org/10.1080/10473289.2004.10470975.
Zhu, C., Farah, J., Choël, M., Gosselin, S., Baroudi, M., Petitprez, D., et al. (2018). Uptake of ozone and modification of lipids in Betula Pendula pollen. Environmental Pollution, 242, 880–886. https://doi.org/10.1016/j.envpol.2018.07.025.
Žiarovská, J., Labajová, M., Ražná, K., Bežo, M., Štefúnová, V., Shevtsova, T., et al. (2013). Changes in expression of betv1 allergen of silver birch pollen in urbanized area of Ukraine. Journal of Environmental Science and Health, Part A, 48(12), 1479–1484. https://doi.org/10.1080/10934529.2013.796788.
Acknowledgements
MC and NV thank the University of Lille and the Institut de Recherches Pluridisciplinaires en Sciences de l’Environnement (IREPSE Fed 4129) for financial support. The CaPPA project (Chemical and Physical Properties of the Atmosphere) is funded by the French National Research Agency (ANR) through the PIA (Programme d'Investissement d'Avenir) under contract ANR-11-LABX-005-01. This work is a contribution to the CPER research project CLIMIBIO. The authors thank the French Ministère de l'Enseignement Supérieur et de la Recherche, the Hauts-de-France Region and the European Funds for Regional Economic Development for their financial support to this project.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Choël, M., Ivanovsky, A., Roose, A. et al. Evaluation of hirst-type sampler and PM10 impactor for investigating adhesion of atmospheric particles onto allergenic pollen grains. Aerobiologia 36, 657–668 (2020). https://doi.org/10.1007/s10453-020-09662-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10453-020-09662-8