Abstract
Epidemiological analyses of airborne allergenic pollen often use concentration measurements from a single station to represent exposure across a city, but this approach does not account for the spatial variation of concentrations within the city. Because there are few descriptions of urban-scale variation, the resulting exposure measurement error is unknown but potentially important for epidemiological studies. This study examines urban-scale variation in pollen concentrations by measuring pollen concentrations of 13 taxa over 24-h periods twice weekly at 25 sites in two seasons in Detroit, Michigan. Spatiotemporal variation is described using cumulative distribution functions and regression models. Daily pollen concentrations across the 25 stations varied considerably, and the average quartile coefficient of dispersion was 0.63. Measurements at a single site explained 3–85% of the variation at other sites, depending on the taxon, and 95% prediction intervals of pollen concentrations generally spanned one to two orders of magnitude. These results demonstrate considerable heterogeneity of pollen levels at the urban scale and suggest that the use of a single monitoring site will not reflect pollen exposure over an urban area and can lead to sizable measurement error in epidemiological studies, particularly when a daily time step is used. These errors might be reduced by using predictive daily pollen levels in models that combine vegetation maps, pollen production estimates, phenology models, and dispersion processes, or by using coarser time steps in the epidemiological analysis.
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References
Adams-Groom, B., Skjoth, C. A., Baker, M., & Welch, T. E. (2017). Modelled and observed surface soil pollen deposition distance curves for isolated trees of Carpinus betulus, Cedrus atlantica, Juglans nigra and Platanus acerifolia. Aerobiologia, 33(3), 1–10. https://doi.org/10.1007/s10453-017-9479-1.
Auer, C., Meyer, T., & Sagun, V. (2016). Reducing pollen dispersal using forest windbreaks. Plant Science Articles.
Blaiss, M. S., Hammerby, E., Robinson, S., Kennedy-Martin, T., & Buchs, S. (2018). The burden of allergic rhinitis and allergic rhinoconjunctivitis on adolescents: A literature review. Annals of Allergy, Asthma & Immunology, 121(1), 43–52.e3. https://doi.org/10.1016/j.anai.2018.03.028.
Bonett, D. G. (2006). Confidence interval for a coefficient of quartile variation. Computational Statistics & Data Analysis, 50(11), 2953–2957. https://doi.org/10.1016/j.csda.2005.05.007.
Borrell, J. S. (2012). Rapid assessment protocol for pollen settling velocity: Implications for habitat fragmentation. Bioscience Horizons, 5, 1–9. https://doi.org/10.1093/biohorizons/hzs002.
Bousquet, J., Khaltaev, N., Cruz, A. A., Denburg, J., Fokkens, W. J., Togias, A., et al. (2008). Allergic Rhinitis and its Impact on Asthma (ARIA) 2008 update (in collaboration with the World Health Organization, GA2LEN and AllerGen). Allergy: European Journal of Allergy and Clinical Immunology, 63(86), 8–160. https://doi.org/10.1111/j.1398-9995.2007.01620.x.
Brennan, G. L., Potter, C., de Vere, N., Griffith, G. W., Skjøth, C. A., Osborne, N. J., et al. (2019). Temperate airborne grass pollen defined by spatio-temporal shifts in community composition. Nature Ecology and Evolution, 3(May), 750–754. https://doi.org/10.1038/s41559-019-0849-7.
Bricchi, E., Frenguelli, G., & Mincigrucci, G. (2000). Experimental results about Platanus pollen deposition. Aerobiologia, 16, 347–352. Retrieved December 13, 2013, from http://link.springer.com/article/10.1023/A:1026701028901.
Cardell, L. O., Olsson, P., Andersson, M., Welin, K. O., Svensson, J., Tennvall, G. R., et al. (2016). TOTALL: High cost of allergic rhinitis—a national Swedish population-based questionnaire study. Primary Care Respiratory Medicine, 26(15082), 1–5. https://doi.org/10.1038/npjpcrm.2015.82.
Charalampopoulos, A., Lazarina, M., Tsiripidis, I., & Vokou, D. (2018). Quantifying the relationship between airborne pollen and vegetation in the urban environment. Aerobiologia, 34(3), 1–16. https://doi.org/10.1007/s10453-018-9513-y.
D’Amato, G., Cecchi, L., Bonini, S., Nunes, C., Annesi-Maesano, I., Behrendt, H., et al. (2007). Allergenic pollen and pollen allergy in Europe. Allergy, 62(9), 976–990. https://doi.org/10.1111/j.1398-9995.2007.01393.x.
Darrow, L. A., Hess, J., Rogers, C. A., Tolbert, P. E., Klein, M., & Sarnat, S. E. (2012). Ambient pollen concentrations and emergency department visits for asthma and wheeze. The Journal of Allergy and Clinical Immunology, 130(3), 630–638.e4. https://doi.org/10.1016/j.jaci.2012.06.020.
Di-Giovanni, F. (1998). A review of the sampling efficiency of rotating-arm impactors used in aerobiological studies. Grana, 37(3), 164–171. https://doi.org/10.1080/00173139809362661.
Dionisio, K. L., Baxter, L. K., Burke, J., & Özkaynak, H. (2016). The importance of the exposure metric in air pollution epidemiology studies: When does it matter, and why? Air Quality, Atmosphere and Health, 9(5), 495–502. https://doi.org/10.1007/s11869-015-0356-1.
Emberlin, J., & Norris-Hill, J. (1991). Spatial variation of pollen deposition in North London. Grana, 30(1), 190–195. https://doi.org/10.1080/00173139109427798.
Endsley, K. A., Brown, D. G., & Bruch, E. (2018). Housing market activity is associated with disparities in urban and metropolitan vegetation. Ecosystems, 21(8), 1–15. https://doi.org/10.1007/s10021-018-0242-4.
Erbas, B., Akram, M., Dharmage, S. C., Tham, R., Dennekamp, M., Newbigin, E., et al. (2012). The role of seasonal grass pollen on childhood asthma emergency department presentations. Clinical and Experimental Allergy, 42(5), 799–805. https://doi.org/10.1111/j.1365-2222.2012.03995.x.
Fernández-Rodríguez, S., Tormo-Molina, R., Maya-Manzano, J. M., Silva-Palacios, I., & Gonzalo-Garijo, Á. (2014a). Comparative study of the effect of distance on the daily and hourly pollen counts in a city in the south-western Iberian Peninsula. Aerobiologia, 30(2), 173–187. https://doi.org/10.1007/s10453-013-9316-0.
Fernández-Rodríguez, S., Tormo-Molina, R., Maya-Manzano, J. M., Silva-Palacios, I., & Gonzalo-Garijo, Á. (2014b). A comparative study on the effects of altitude on daily and hourly airborne pollen counts. Aerobiologia, 30(3), 257–268. https://doi.org/10.1007/s10453-014-9325-7.
Frenz, D. A. (2000). The effect of windspeed on pollen and spore counts collected with the Rotorod Sampler and Burkard spore trap. Annals of Allergy, Asthma & Immunology, 85(5), 392–394. https://doi.org/10.1016/S1081-1206(10)62553-7.
Frenz, D. A. (2001). Interpreting atmospheric pollen counts for use in clinical allergy: Allergic symptomology. Annals of Allergy, Asthma & Immunology, 86(2), 150–158. https://doi.org/10.1016/S1081-1206(10)62683-X.
Frenz, D. A., Scamehorn, R. T., Hokanson, J. M., & Murray, L. W. (1996). A brief method for analyzing rotorod samples for pollen content. Aerobiologia, 12, 51–54.
Gleason, J. A., Bielory, L., & Fagliano, J. A. (2014). 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. Environmental Research, 132, 421–429. https://doi.org/10.1016/j.envres.2014.03.035.
Gräler, B., Pebesma, E., & Heuvelink, G. (2016). Spatio-temporal interpolation using gstat. The R Journal, 8(1), 204–218.
Groffman, P. M., Cavender-Bares, J., Bettez, N. D., Grove, J. M., Hall, S. J., Heffernan, J. B., et al. (2014). Ecological homogenization of urban USA. Frontiers in Ecology and the Environment, 12(1), 74–81. https://doi.org/10.1890/120374.
Guilbert, A., Simons, K., Hoebeke, L., Packeu, A., Hendrickx, M., De Cremer, K., et al. (2016). Short-term effect of pollen and spore exposure on allergy morbidity in the Brussels-Capital Region. EcoHealth, 13(2), 303–315. https://doi.org/10.1007/s10393-016-1124-x.
Hepworth, W., Vinay, P., & Zenger, V. (1983). Airborne and allergenic pollen of North America. Airborne and Allergenic Pollen of North America. Baltimore: Johns Hopkins University Press.
Hernández-Ceballos, M. A., García-Mozo, H., Adame, J. A., Domínguez-Vilches, E., Bolívar, J. P., De La Morena, B. A., et al. (2011). Determination of potential sources of Quercus airborne pollen in Cordoba city (southern Spain) using back-trajectory analysis. Aerobiologia, 27(3), 261–276. https://doi.org/10.1007/s10453-011-9195-1.
Hjort, J., Hugg, T. T., Antikainen, H., Rusanen, J., Sofiev, M., Jaakkola, M. S., et al. (2015). Fine-scale exposure to allergenic pollen in the urban environment: Evaluation of land use regression approach. Environmental Health Perspectives, 124(5), 619–626. https://doi.org/10.1289/ehp.1509761.
Huang, H., Ye, R., Qi, M., Li, X., Miller, D. R., Stewart, C. N., et al. (2015). Wind-mediated horseweed (Conyza canadensis) gene flow: Pollen emission, dispersion, and deposition. Ecology and Evolution, 5(13), 2646–2658. https://doi.org/10.1002/ece3.1540.
Hugg, T., & Rantio-Lehtimäki, A. (2007). Indoor and outdoor pollen concentrations in private and public spaces during the Betula pollen season. Aerobiologia, 23(2), 119–129. https://doi.org/10.1007/s10453-007-9057-z.
Ishibashi, Y., Ohno, H., Oh-ishi, S., Matsuoka, T., Kizaki, T., & Yoshizumi, K. (2008). Characterization of pollen dispersion in the neighborhood of Tokyo, Japan in the spring of 2005 and 2006. International Journal of Environmental Research and Public Health, 5(1), 76–85. https://doi.org/10.3390/ijerph5020076.
Ito, K., Weinberger, K. R., Robinson, G. S., Sheffield, P. E., Lall, R., Mathes, R., et al. (2015). The associations between daily spring pollen counts, over-the-counter allergy medication sales, and asthma syndrome emergency department visits in New York City, 2002–2012. Environmental Health, 14(1), 71. https://doi.org/10.1186/s12940-015-0057-0.
Kahle, D., & Wickham, H. (2013). ggmap: Spatial visualization with ggplot2. The R Journal, 5(1), 144–161.
Katz, D. S. W., & Batterman, S. A. (2019). Allergenic pollen production across a large city for common ragweed (Ambrosia artemisiifolia). Landscape and Urban Planning, 190(March), 103615. https://doi.org/10.1016/j.landurbplan.2019.103615.
Katz, D. S. W., & Carey, T. S. (2014). Heterogeneity in ragweed pollen exposure is determined by plant composition at small spatial scales. Science of the Total Environment, 485, 435–440. https://doi.org/10.1016/j.scitotenv.2014.03.099.
Katz, D. S. W., Dzul, A., Kendel, A., & Batterman, S. A. (2019). Effect of intra-urban temperature variation on tree flowering phenology, airborne pollen, and measurement error in epidemiological studies of allergenic pollen. Science of the Total Environment, 653, 1213–1222. https://doi.org/10.1016/j.scitotenv.2018.11.020.
Katz, D. S. W., Morris, J. R., & Batterman, S. A. (2020). Pollen production for 13 urban North American tree species: allometric equations for tree trunk diameter and crown area. Aerobiologia. https://doi.org/10.1007/s10453-020-09638-8.
Klein, E., Lavigne, C., Foueillassar, X., Gouyon, P., & Laredo, C. (2003). Corn pollen dispersal: Quasi-mechanistic models and field experiments. Ecological Monographs, 73(1), 131–150.
Kuparinen, A. (2006). Mechanistic models for wind dispersal. Trends in Plant Science, 11(6), 296–301. https://doi.org/10.1016/j.tplants.2006.04.006.
La Rosa, M., Lionetti, E., Reibaldi, M., Russo, A., Longo, A., Leonardi, S., et al. (2013). Allergic conjunctivitis: A comprehensive review of the literature. Italian Journal of Pediatrics, 39, 18. https://doi.org/10.1186/1824-7288-39-18.
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.
Linneberg, A., Henrik Nielsen, N., Frølund, L., Madsen, F., Dirksen, A., & Jørgensen, T. (2002). The link between allergic rhinitis and allergic asthma: A prospective population-based study. The Copenhagen Allergy Study. Allergy: European Journal of Allergy and Clinical Immunology, 57(11), 1048–1052. https://doi.org/10.1034/j.1398-9995.2002.23664.x.
Martin, M. D., Chamecki, M., & Brush, G. S. (2010). Anthesis synchronization and floral morphology determine diurnal patterns of ragweed pollen dispersal. Agricultural and Forest Meteorology, 150(9), 1307–1317. https://doi.org/10.1016/j.agrformet.2010.06.001.
Maya-Manzano, J. M., Sadyś, M., Tormo-Molina, R., Fernández-Rodríguez, S., Oteros, J., Silva-Palacios, I., et al. (2017). Relationships between airborne pollen grains, wind direction and land cover using GIS and circular statistics. Science of the Total Environment. https://doi.org/10.1016/j.scitotenv.2017.01.085.
Meltzer, E. O. (2016). Allergic rhinitis: Burden of illness, quality of life, comorbidities, and control. Immunology and Allergy Clinics of North America, 36(2), 235–248. https://doi.org/10.1016/j.iac.2015.12.002.
Meltzer, E. O., Blaiss, M. S., Derebery, M. J., Mahr, T. A., Gordon, B. R., Sheth, K. K., et al. (2009). Burden of allergic rhinitis: Results from the Pediatric Allergies in America survey. Journal of Allergy and Clinical Immunology, 124(3 SUPPL. 1), 43–70. https://doi.org/10.1016/j.jaci.2009.05.013.
Miki, K., Kawashima, S., Fujita, T., Nakamura, K., & Clot, B. (2017). Effect of micro-scale wind on the measurement of airborne pollen concentrations using volumetric methods on a building rooftop. Atmospheric Environment, 158, 1–10. https://doi.org/10.1016/j.atmosenv.2017.03.015.
Mims, J. W. (2014). Epidemiology of allergic rhinitis. International Forum of Allergy and Rhinology, 4(SUPPL.2), 18–20. https://doi.org/10.1002/alr.21385.
Nathan, R. (2007). The burden of allergic rhinitis. Allergy and Asthma Proceedings, 28(1), 3–9. https://doi.org/10.2500/aap.2007.28.2934.
Osborne, N. J., Alcock, I., Wheeler, B. W., Hajat, S., Sarran, C., Clewlow, Y., et al. (2017). Pollen exposure and hospitalization due to asthma exacerbations: daily time series in a European city. International Journal of Biometeorology, 61(10), 1837–1848. https://doi.org/10.1007/s00484-017-1369-2.
Peel, R. G., Kennedy, R., Smith, M., & Hertel, O. (2014). Do urban canyons influence street level grass pollen concentrations? International Journal of Biometeorology, 58(6), 1317–1325. https://doi.org/10.1007/s00484-013-0728-x.
Qin, P., Waltoft, B. L., Mortensen, P. B., & Postolache, T. T. (2013). Suicide risk in relation to air pollen counts: a study based on data from Danish registers. British Medical Journal Open, 3(5), e002462. https://doi.org/10.1136/bmjopen-2012-002462.
R Core Team. (2018). R: A language and environment for statistical computing. Vienna: R Core Team.
Rojo, J., Oteros, J., Pérez-badia, R., Cervigón, P., Ferencova, Z., Gutiérrez-bustillo, A. M., et al. (2019). Near-ground effect of height on pollen exposure. Environmental Research. https://doi.org/10.1016/j.envres.2019.04.027.
Roman, L. A., Pearsall, H., Eisenman, T. S., Conway, T. M., Fahey, R. T., Landry, S., et al. (2018). Human and biophysical legacies shape contemporary urban forests: A literature synthesis. Urban Forestry and Urban Greening, 31(December 2017), 157–168. https://doi.org/10.1016/j.ufug.2018.03.004.
Sakata, S., Konishi, S., Ng, C. F. S., Kishikawa, R., & Watanabe, C. (2017). Association of Asian Dust with daily medical consultations for pollinosis in Fukuoka City, Japan. Environmental Health and Preventive Medicine, 22(1), 25. https://doi.org/10.1186/s12199-017-0623-x.
Salo, P., Calatroni, A., Gergen, P., Hoppin, J., Sever, M., Jaramillo, R., et al. (2011). Allergy-related outcomes in relation to serum IgE: Results from the National Health and Nutrition Examination Survey 2005–2006. Journal of Allergy and Clinical Immunology, 127(5), 1226–1235. https://doi.org/10.1016/j.jaci.2010.12.1106.Allergy-related.
Skjøth, C. A., Ørby, P. V., Becker, T., Geels, C., Schlünssen, V., Sigsgaard, T., et al. (2013). Identifying urban sources as cause of elevated grass pollen concentrations using GIS and remote sensing. Biogeosciences, 10(1), 541–554. https://doi.org/10.5194/bg-10-541-2013.
Smith, G. (1984). Sampling and identifying allergenic pollens and moulds. San Antonio: Blewstone Press.
Soldevilla, C. G., Alcfizar-Teno, P., & Dominguez-Vilches, E. (1995). Airborne pollen grain concentrations at two different heights. Aerobiologia Aerobiologia Internalional Journal of Aerobiology, 11, 105–109. https://doi.org/10.1007/BF02738275.
Spieksma, F. T. M., Van Noort, P., & Nikkels, H. (2000). Influence of nearby stands of Artemisia on street-level versus roof-top-level ratio’s of airborne pollen quantities. Aerobiologia, 16(1), 21–24. https://doi.org/10.1023/A:1007618017071.
Sun, X., Waller, A., Yeatts, K. B., & Thie, L. (2016). Pollen concentration and asthma exacerbations in Wake County, North Carolina, 2006–2012. Science of the Total Environment, 544, 185–191. https://doi.org/10.1016/j.scitotenv.2015.11.100.
Wang, J., Qi, M., Huang, H., Ye, R., Li, X., & Neal Stewart, C. (2017). Atmospheric pollen dispersion from herbicide-resistant horseweed (Conyza canadensis L.). Aerobiologia, 33(3), 393–406. https://doi.org/10.1007/s10453-017-9477-3.
Wang, K., Wang, T., & Liu, X. (2019). A review: Individual tree species classification using integrated airborne LiDAR and optical imagery with a focus on the urban environment. Forests, 10(1), 1–18. https://doi.org/10.3390/f10010001.
Weinberger, K. R., Kinney, P. L., & Lovasi, G. S. (2015). A review of spatial variation of allergenic tree pollen within cities. Arboriculture & Urban Forestry, 41(2), 57–68.
Weinberger, K. R., Kinney, P. L., Robinson, G. S., Sheehan, D., Kheirbek, I., Matte, T. D., et al. (2018). Levels and determinants of tree pollen in New York City. Journal of Exposure Science & Environmental Epidemiology, 28(2), 119–124. https://doi.org/10.1038/jes.2016.72.
Werchan, B., Werchan, M., Mücke, H. G., & Bergmann, K. C. (2018). Spatial distribution of pollen-induced symptoms within a large metropolitan area—Berlin, Germany. Aerobiologia, 34(4), 539–556. https://doi.org/10.1007/s10453-018-9529-3.
Werchan, B., Werchan, M., Mücke, H.-G., Gauger, U., Simoleit, A., Zuberbier, T., et al. (2017). Spatial distribution of allergenic pollen through a large metropolitan area. Environmental Monitoring and Assessment, 189(4), 169. https://doi.org/10.1007/s10661-017-5876-8.
Wickham, H. (2016). ggplot2: Elegant graphics for data analysis. New York, NY: Springer. https://ggplot2.tidyverse.org. Accessed 1 Jan 2018
Wilson, J. G., Kingham, S., Pearce, J., & Sturman, A. P. (2005). A review of intraurban variations in particulate air pollution: Implications for epidemiological research. Atmospheric Environment, 39(34), 6444–6462. https://doi.org/10.1016/j.atmosenv.2005.07.030.
Acknowledgements
This work was supported by the National Institute of Environmental Health Sciences through a NRSA postdoctoral fellowship (Grant Number F32 ES026477). It was also supported by the Michigan Institute for Clinical Health Research through the Postdoctoral Translational Scholars Program (Grant Number UL1 TR002240). S. Batterman also acknowledges support from Grant P30ES017885 from the National Institute of Environmental Health Sciences, National Institutes of Health. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. We thank John Kost for his considerable effort on this project and the volunteers that allowed us to sample pollen on their property.
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Katz, D.S.W., Batterman, S.A. Urban-scale variation in pollen concentrations: a single station is insufficient to characterize daily exposure. Aerobiologia 36, 417–431 (2020). https://doi.org/10.1007/s10453-020-09641-z
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DOI: https://doi.org/10.1007/s10453-020-09641-z