Abstract
Alternaria and Cladosporium are the most common airborne fungal spores responsible for health problems, as well as for crop pathologies. The study of their behavior in the air is a necessary step for establishing control and prevention measures. The aim of this paper is to develop a logistic regression model for predicting the daily concentrations of airborne Alternaria and Cladosporium fungal spores from meteorological variables. To perform the logistic regression analysis, the concentration levels are binarized using concentration thresholds. The fungal spore data have been obtained at eight aerobiological monitoring stations of the Aerobiological Network of Catalonia (NE Spain). The meteorological data used were the maximum and minimum daily temperatures and daily rainfall provided by the meteorological services. The relationship between the meteorological variables and the fungal spore levels has been modeled by means of logistic regression equations, using data from the period 1995–2012. Values from years 2013–2014 were used for validation. In the case of Alternaria, three equations for predicting the presence and the exceedance of the thresholds 10 and 30 spores/m3 have been established. For Cladosporium, four equations for the thresholds 200, 500, 1000, and 1500 spores/m3 have been established. The temperature and cumulative rainfall in the last 3 days showed a positive correlation with airborne fungal spore levels, while the rain on the same day had a negative correlation. Sensitivity and specificity were calculated to measure the predictive power of the model, showing a reasonable percentage of correct predictions (ranging from 48 to 99%). The simple equations proposed allow us to forecast the levels of fungal spores that will be in the air the next day, using only the maximum and minimum temperatures and rainfall values provided by weather forecasting services.
Similar content being viewed by others
References
Allue Andrade JL (1990) Phytoclimatic atlas of Spain. Taxonomies. Instituto Nacional de Investigaciones Agrarias, Ministerio de Agricultura, Pesca y Alimentación, Madrid, España
Almeida E, Caeiro E, Todo-Bom A, Ferro R, Dionísio A, Duarte A, Gazarini L (2018) The influence of meteorological parameters on Alternaria and Cladosporium fungal spore concentrations in Beja (Southern Portugal): preliminary results. Aerobiologia 34:219–226. https://doi.org/10.1007/s10453-018-9508-8
Astray G, Rodríguez-Rajo FJ, Ferreiro-Lage JA, Fernández-González M, Jato V, Mejuto JC (2010) The use of artificial neural networks to forecast biological atmospheric allergens or pathogens only as Alternaria spores. J Environ Monit 12:2145–2152. https://doi.org/10.1039/C0EM00248H
Barbosa AM, Real R, Olivero J, Vargas JM (2003) Otter (Lutra lutra) distribution modeling at two resolution scales suited to conservation planning in the Iberian Peninsula. Biol Conserv 114:377–387. https://doi.org/10.1016/S0006-3207(03)00066-1
Barkai-Golan R (2008) Alternaria mycotoxins. In: Barkai-Golan R, Paster N (eds) Mycotoxins in fruits and vegetables. Academic Press, San Diego, EEUU, pp 185–204
Bartra J, Belmonte J, Torres-Rodríguez JM, Cistero-Bahima A (2009) Sensitization to Alternaria in patients with respiratory allergy. Front Biosci Landmark Ed 14:3372–3379. https://doi.org/10.2741/3459
Brito C, Crespo EG, Paulo OS (1999) Modelling wildlife distributions: logistic multiple regression vs overlap analysis. Ecography 22:251–260. https://doi.org/10.1111/j.1600-0587.1999.tb00500.x
Bruno AA, Pace L, Tomassetti B, Coppola E, Verdecchia M, Pacioni G, Visconti G (2007) Estimation of fungal spore concentrations associated to meteorological variables. Aerobiologia 23:221–228. https://doi.org/10.1007/s10453-007-9066-y
Burch M, Levetin E (2002) Effects of meteorological conditions on spore plumes. Int J Biometeorol 46:107–117. https://doi.org/10.1007/s00484-002-0127-1
Chiba S, Okada S, Suzuki Y, Watanuki Z, Mitsuishi Y, Igusa R, Sekii T, Uchiyama B (2009) Cladosporium species-related hypersensitivity pneumonitis in household environments. Intern Med 48:363–367. https://doi.org/10.2169/internalmedicine.48.1811
Corden JM, Millington WM (2001) The long-term trends and seasonal variation of the aeroallergen Alternaria in Derby, UK. Aerobiologia 17:127–136. https://doi.org/10.1023/A:1010876917512
Crawford JA, Rosenbaum PF, Anagnost SE, Hunt A, Abraham JL (2015) Indicators of airborne fungal concentrations in urban homes: understanding the conditions that affect indoor fungal exposures. Sci Total Environ 517:113–124. https://doi.org/10.1016/j.scitotenv.2015.02.060
D’Amato G, Chatzigeorgiou G, Corsico R, Gioulekas D, Jäger L, Jäger S, Kontou-Fili K, Kouridakis S, Liccardi G, Meriggi A, Palma-Carlos A, Palma-Carlos ML, Aleman AP, Parmiani S, Puccinelli P, Russo M, Spieksma FTM, Torricelli R, Wuthrich B (1997) Evaluation of the prevalence of skin prick test positivity to Alternaria and Cladosporium in patients with suspected respiratory allergy. Allergy 52:711–716. https://doi.org/10.1111/j.1398-9995.1997.tb01227.x
Damialis A, Gioulekas D (2006) Airborne allergenic fungal spores and meteorological factors in Greece: forecasting possibilities. Grana 45:122–129. https://doi.org/10.1080/00173130600601005
Damialis A, Mohammad AB, Halley JM, Gange AC (2015) Fungi in a changing world: growth rates will be elevated, but spore production may decrease in future climates. Int J Biometeorol 59:1157–1167. https://doi.org/10.1007/s00484-014-0927-0
De Linares C, Belmonte J, Canela M, Díaz de la Guardia C, Alba-Sanchez F, Sabariego S, Alonso-Pérez S (2010) Dispersal patterns of Alternaria conidia in Spain. Agric For Meteorol 150:1491–1500. https://doi.org/10.1016/j.agrformet.2010.07.004
de Wit PJGM, van der Burgt A, Ökmen B, Stergiopoulos I, Abd-Elsalam KA, Aerts AL, Bahkali AH, Beenen HG, Chettri P, Cox MP, Datema E, de Vries RP, Dhillon B, Ganley AR, Griffiths SA, Guo Y, Hamelin RC, Henrissat B, Kabir MS, Jashni MK, Kema G, Klaubauf S, Lapidus A, Levasseur A, Lindquist E, Mehrabi R, Ohm RA, Owen TJ, Salamov A, Schwelm A, Schijlen E, Sun H, van den Burg HA, van Ham RCHJ, Zhang S, Goodwin SB, Grigoriev IV, Collemare J, Bradshaw RE (2012) The genomes of the fungal plant pathogens Cladosporium fulvum and Dothistroma septosporum reveal adaptation to different hosts and lifestyles but also signatures of common ancestry. PLoS Genet 8:e1003088. https://doi.org/10.1371/journal.pgen.1003088
Escuredo O, Seijo MC, Fernández-González M, Iglesias I (2011) Effects of meteorological factors on the levels of Alternaria spores on a potato crop. Int J Biometeorol 55:243–252. https://doi.org/10.1007/s00484-010-0330-4
Fitt BDL, McCartney HA, Walklate PJ (1989) The role of rain in dispersal of pathogen inoculum. Annu Rev Phytopathol 27:241–270. https://doi.org/10.1146/annurev.py.27.090189.001325
Frankland AW, Davies RR (1965) Allergie aux spores de moisissures en Angleterre. Poumon Coeur 21:11–23
Galán C, Cariñanos P, Alcázar P, Dominguez E (2007) Manual de calidad y gestión de la Red Española de Aerobiología. Universidad de Córdoba, Cordoba
Galán C, Ariatti A, Bonini M, Clot B, Crouzy B, Dahl A, Fernandez-González D, Frenguelli G, Gehrig R, Isard S, Levetin E, Li DW, Mandrioli P, Rogers CA, Thibaudon M, Sauliene I, Skjoth C, Smith M, Sofiev M (2017) Recommended terminology for aerobiological studies. Aerobiologia 33:293–295. https://doi.org/10.1007/s10453-017-9496-0
Gianni C, Cerri A, Crosti C (1997) Ungual phaeohyphomycosis caused by Alternaria alternata. Mycoses 40:219–221. https://doi.org/10.1111/j.1439-0507.1997.tb00218.x
Green BJ, Tovey ER, Sercombe JK, Blachere FM, Beezhold DH, Schmechel D (2006) Airborne fungal fragments and allergenicity. Med Mycol 44:S245–S255. https://doi.org/10.1080/13693780600776308
Grinn-Gofroń A, Bosiacka B (2015) Effects of meteorological factors on the composition of selected fungal spores in the air. Aerobiologia 31:63–72. https://doi.org/10.1007/s10453-014-9347-1
Grinn-Gofroń A, Rapiejko P (2009) Occurrence of Cladosporium spp. and Alternaria spp. spores in Western, Northern and Central-Eastern Poland in 2004–2006 and relation to some meteorological factors. Atmos Res 93:747–758. https://doi.org/10.1016/j.atmosres.2009.02.014
Grinn-Gofroń A, Strzelczak A (2008) Artificial neural network models of relationships between Alternaria spores and meteorological factors in Szczecin (Poland). Int J Biometeorol 52:859–868. https://doi.org/10.1007/s00484-008-0182-3
Grinn-Gofroń A, Strzelczak A (2013) Changes in concentration of Alternaria and Cladosporium spores during summer storms. Int J Biometeorol 57:759–768. https://doi.org/10.1007/s00484-012-0604-0
Grinn-Gofroń A, Nowosad J, Bosiacka B, Camacho I, Pashley C, Belmonte J, De Linares C, Ianovici N, Manzano JMM, Sadyś M, Skjøth C, Rodinkova V, Tormo-Molina R, Vokou D, Fernández-Rodríguez S, Damialis A (2019) Airborne Alternaria and Cladosporium fungal spores in Europe: forecasting possibilities and relationships with meteorological parameters. Sci Total Environ 653:938–946. https://doi.org/10.1016/j.scitotenv.2018.10.419
Gugnani HC, Ramesh V, Sood N, Guarro J, Moin-Ul-Haq, Paliwal-Joshi A, Singh B, Makkar R (2006) Cutaneous phaeohyphomycosis caused by Cladosporium oxysporum and its treatment with potassium iodide. Med Mycol 44:285–288. https://doi.org/10.1080/13693780500294824
Hirst JM (1952) An automatic volumetric spore trap. Ann Appl Biol 39:257–265. https://doi.org/10.1111/j.1744-7348.1952.tb00904.x
Hollins PD, Kettlewell PS, Atkinson MD, Stephenson DB, Corden JM, Millington WM, Mullins J (2004) Relationships between airborne fungal spore concentration of Cladosporium and the summer climate at two sites in Britain. Int J Biometeorol 48:137–141. https://doi.org/10.1007/s00484-003-0188-9
Hosmer DW, Lemeshow S (2000) Multiple logistic regression. In: Wiley Series in Probability and Statistics Texts and References Section, second edn. John Wiley & Sons, Inc., Hoboken EEUU
Huyan X-H, Yang Y-P, Fan Y-M, Huang W-M, Li W, Zhou Y (2012) Cutaneous and systemic pathogenicity of a clinical isolate of Cladosporium sphaerospermum in a murine model. J Comp Pathol 147:354–359. https://doi.org/10.1016/j.jcpa.2012.01.023
Ianovici N, Dumbravă-Dodoacă M, Filimon MN, Sinitean A (2011) A comparative aeromycological study of the incidence of allergenic spores in outdoor environment. Analele Univ Din Oradea Fasc Biol 18:88–98
Kasprzyk I (2008) Aeromycology–main research fields of interest during the last 25 years. Ann Agric Environ Med 15(1):1–7
Kasprzyk I, Kaszewski BM, Weryszko-Chmielewska E, Nowak M, Sulborska A, Kaczmarek J, Szymanska A, Haratym W, Jedryczka M (2016) Warm and dry weather accelerates and elongates Cladosporium spore seasons in Poland. Aerobiologia 32:109–126. https://doi.org/10.1007/s10453-016-9425-7
Kirk PM, Cannon PF, Minter DW, Stalpers JA (2008) Dictionary of the Fungi, 10th edn. CABI, Wallingford
Knutsen AP, Bush RK, Demain JG, Denning DW, Dixit A, Fairs A, Greenberger PA, Kariuki B, Kita H, Kurup VP, Moss RB, Niven RM, Pashley CH, Slavin RG, Vijay HM, Wardlaw AJ (2012) Fungi and allergic lower respiratory tract diseases. J Allergy Clin Immunol 129:280–291. https://doi.org/10.1016/j.jaci.2011.12.970
Kurkela T (1997) The number of Cladosporium conidia in the air in different weather conditions. Grana 36:54–61. https://doi.org/10.1080/00173139709362591
Kurup VP, Shen H-D, Vijay H (2002) Immunobiology of fungal allergens. Int Arch Allergy Immunol 129:181–188. https://doi.org/10.1159/000066780
Latorre BA, Briceño EX, Torres R (2011) Increase in Cladosporium spp. populations and rot of wine grapes associated with leaf removal. Crop Prot 30:52–56. https://doi.org/10.1016/j.cropro.2010.08.022
Lewis SA, Corden JM, Forster GE, 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. Clin Exp Allergy 30:1724–1732. https://doi.org/10.1046/j.1365-2222.2000.00947.x
Logrieco A, Bottalico A, Mulé G, Moretti A, Perrone G (2003) Epidemiology of toxigenic fungi and their associated mycotoxins for some Mediterranean crops. Eur J Plant Pathol 109:645–667. https://doi.org/10.1023/A:1026033021542
Machin, D., Campbell, M.J., Walters, S.J., 2007. Medical statistics
Molina AM, Romero JA, García-Pantaleón FI, Comtois P, Vilches ED (1998) Preliminary statistical modeling of the presence of two conidial types of Cladosporium in the atmosphere of Córdoba, Spain. Aerobiologia 14:229–234. https://doi.org/10.1007/BF02694211
Myers RH (1990) Classical and modern regression with applications. Duxbury Press Belmont, CA
Ogórek R, Lejman R, Pusz W, Miłluch A, Miodyńska P (2012) Characteristics and taxonomy of Cladosporium fungi. Mikol Lek 19:80–85
Ojeda P, Sastre J, Olaguibel JM, Chivato T (2018) Alergológica 2015: a national survey on allergic diseases in the adult Spanish population. J Investig Allergol Clin Immunol 28(3):151–164
Oliveira M, Ribeiro H, Delgado J, Abreu I (2009a) Aeromycological profile of indoor and outdoor environments. J Environ Monit 11:1360–1367. https://doi.org/10.1039/B820736D
Oliveira M, Ribeiro H, Delgado J, Abreu I (2009b) The effects of meteorological factors on airborne fungal spore concentration in two areas differing in urbanisation level. Int J Biometeorol 53:61–73. https://doi.org/10.1007/s00484-008-0191-2
Peteira B, Bernal Cabrera A, Martínez B, Ileana M (2011) Caracterización molecular de aislamientos de Cladosporium fulvum Cooke provenientes de tomate en condiciones de cultivo protegido. Rev Protección Veg 26:5–14
Peternel R, Culig J, Hrga I (2004) Atmospheric concentrations of Cladosporium spp. and Alternaria spp. sporesin Zagreb (Croatia) and effects of some meteorological factors. Ann Agric Environ Med 11:303–307
Petraitis PS, Dunham AE, Niewiarowski PH (1996) Inferring multiple causality: the limitations of path analysis. Funct Ecol 10:421–431
Qiu-Xia C, Chang-Xing L, Wen-Ming H, Jiang-Qiang S, Wen L, Shun-Fang L (2008) Subcutaneous phaeohyphomycosis caused by Cladosporium sphaerospermum. Mycoses 51:79–80. https://doi.org/10.1111/j.1439-0507.2007.01417.x
Recio M, Trigo MM, Docampo S, Melgar M, García-Sánchez J, Bootello L, Cabezudo B (2012) Analysis of the predicting variables for daily and weekly fluctuations of two airborne fungal spores: Alternaria and Cladosporium. Int J Biometeorol 56:983–991. https://doi.org/10.1007/s00484-011-0509-3
Revankar SG, Sutton DA (2010) Melanized fungi in human disease. Clin Microbiol Rev 23:884–928. https://doi.org/10.1128/CMR.00019-10
Reyes ES, de la Cruz DR, Merino ES, Sánchez JS (2009) Meteorological and agricultural effects on airborne Alternaria and Cladosporium spores and clinical aspects in Valladolid [Spain]. Ann Agric Environ Med 16:53–61
Rodríguez-Rajo FJ, Iglesias I, Jato V (2005) Variation assessment of airborne Alternaria and Cladosporium spores at different bioclimatical conditions. Mycol Res 109:497–507
Rojas AB, Cotilla I, Real R, Palomo LJ (2001) Determinación de las áreas probables de distribución de los mamíferos terrestres en la provincia de Málaga. Galemys 13:217–229
Romano C, Bilenchi R, Alessandrini C, Miracco C (1999) Case Report. Cutaneous phaeohyphomycosis caused by Cladosporium oxysporum. Mycoses 42:111–115. https://doi.org/10.1046/j.1439-0507.1999.00263.x
Sanchez H, Bush RK (2001) A review of Alternaria alternata sensitivity. Rev Iberoam Micol 18:56–59
Sindt C, Besancenot J-P, Thibaudon M (2016) Airborne Cladosporium fungal spores and climate change in France. Aerobiologia 32:53–68. https://doi.org/10.1007/s10453-016-9422-x
Sociedad Española de Alergología e Inmunología Clínica, G.A (2017) Alergológica 2015: Factores epidemiológicos, clínicos y socioeconómicos de la enfermedad alérgica en España en 2015. Grupo de Comunicación Healthcare, Madrid
Sousa L, Camacho IC, Grinn-Gofroń A, Camacho R (2016) Monitoring of anamorphic fungal spores in Madeira region (Portugal), 2003–2008. Aerobiologia 32:303–315. https://doi.org/10.1007/s10453-015-9400-8
Stępalska D, Wołek J (2005) Variation in fungal spore concentrations of selected taxa associated. Aerobiologia 21:43–52. https://doi.org/10.1007/s10453-004-5877-2
Suits DB (1984) Dummy variables: mechanics V. Interpretation. Rev Econ Stat 66:177–180. https://doi.org/10.2307/1924713
Targonski PV, Persky VW, Ramekrishnan V (1995) Effect of environmental molds on risk of death from asthma during the pollen season. J Allergy Clin Immunol 95:955–961. https://doi.org/10.1016/S0091-6749(95)70095-1
Teixeira J, Ferrand N, Arntzen JW (2001) Biogeography of the golden-striped salamander Chioglossa lusitanica: a field survey and spatial modelling approach. Ecography 24:618–624. https://doi.org/10.1111/j.1600-0587.2001.tb00495.x
Thomma BPHJ (2003) Alternaria spp.: from general saprophyte to specific parasite. Mol Plant Pathol 4:225–236. https://doi.org/10.1046/j.1364-3703.2003.00173.x
Troutt C, Levetin E (2001) Correlation of spring spore concentrations and meteorological conditions in Tulsa, Oklahoma. Int J Biometeorol 45:64–74. https://doi.org/10.1007/s004840100087
van der Waals JE, Korsten L, Aveling TAS, Denner FDN (2003) Influence of environmental factors on field concentrations of Alternaria solani conidia above a South African potato crop. Phytoparasitica 31:353–364. https://doi.org/10.1007/BF02979806
Vélez-Pereira AM, De Linares C, Delgado R, Belmonte J (2016) Temporal trends of the airborne fungal spores in Catalonia (NE Spain), 1995–2013. Aerobiologia 32:23–37. https://doi.org/10.1007/s10453-015-9410-6
Vieira MR, Milheiro A, Pacheco FA (2001) Phaeohyphomycosis due to Cladosporium cladosporioides. Med Mycol 39:135–137. https://doi.org/10.1080/mmy.39.1.135.137
Wijnand E (2009) Fungal spores: a critical review of the toxicological and epidemiological evidence as a basis for occupational exposure limit setting. Crit Rev Toxicol 39:799–864. https://doi.org/10.3109/10408440903307333
Acknowledgments
The authors wish to thank the entities and projects that make possible to obtain the database used in this study: Laboratorios LETI S.A.; Servei Meteorològic de Catalunya; Diputacions de Barcelona, Girona and Tarragona; SCAIC; SEAIC; Stallergenes Iberica; J. Uriach y Cia; European Commission for “ENV4-CT98-0755”; Spanish Ministry of Science and Technology I+D+I for “AMB97-0457-CO7-021,” “REN2001-10659-CO3-01,” “BOS2002-03474,” “CGL2004-21166-E,” “CGL2005-07543/CLI,” “GGL2006-12648-CO3-02,” “CGL2009-11205,” “CGL2012-39523-C02-01,” “CTM2017-89565-C2-1-P,” FEDER “A way to build Europe,” and CONSOLIDER CSD 2007_00067 GRACCIE; and Catalan Government AGAUR for “2005SGR00519,” “2009SGR1102,” “2014SGR1274,” and “2017SGR1692.” This work is contributing to the ICTA “Unit of Excellence” (MinECo, MDM2015-0552). The authors wish to thank the anonymous referees for careful reading and very helpful comments that resulted in an overall improvement of the paper.
Funding
This work was supported by the Spanish Ministry of Science and Technology through the project “CGL2012-39523-C02-01/CLI” and by the Administrative Department of Science, Technology and Innovation-COLCIENCIAS (Colombia) through the doctoral fellowship to Andrés M. Vélez-Pereira.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
ESM 1
(PDF 4584 kb)
Rights and permissions
About this article
Cite this article
Vélez-Pereira, A.M., De Linares, C., Canela, MA. et al. Logistic regression models for predicting daily airborne Alternaria and Cladosporium concentration levels in Catalonia (NE Spain). Int J Biometeorol 63, 1541–1553 (2019). https://doi.org/10.1007/s00484-019-01767-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00484-019-01767-1