International Journal of Biometeorology

, Volume 63, Issue 12, pp 1541–1553 | Cite as

Logistic regression models for predicting daily airborne Alternaria and Cladosporium concentration levels in Catalonia (NE Spain)

  • Andrés M. Vélez-Pereira
  • Concepción De LinaresEmail author
  • Miguel-Angel Canela
  • Jordina Belmonte
Original Paper


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.


Fungal spore dispersal patterns Fungal spore daily concentration levels Prediction model Threshold 



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 information

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.

Supplementary material

484_2019_1767_MOESM1_ESM.pdf (4.5 mb)
ESM 1 (PDF 4584 kb)


  1. Allue Andrade JL (1990) Phytoclimatic atlas of Spain. Taxonomies. Instituto Nacional de Investigaciones Agrarias, Ministerio de Agricultura, Pesca y Alimentación, Madrid, EspañaGoogle Scholar
  2. 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. CrossRefGoogle Scholar
  3. 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. CrossRefGoogle Scholar
  4. 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. CrossRefGoogle Scholar
  5. Barkai-Golan R (2008) Alternaria mycotoxins. In: Barkai-Golan R, Paster N (eds) Mycotoxins in fruits and vegetables. Academic Press, San Diego, EEUU, pp 185–204CrossRefGoogle Scholar
  6. 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. CrossRefGoogle Scholar
  7. Brito C, Crespo EG, Paulo OS (1999) Modelling wildlife distributions: logistic multiple regression vs overlap analysis. Ecography 22:251–260. CrossRefGoogle Scholar
  8. 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. CrossRefGoogle Scholar
  9. Burch M, Levetin E (2002) Effects of meteorological conditions on spore plumes. Int J Biometeorol 46:107–117. CrossRefGoogle Scholar
  10. 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. CrossRefGoogle Scholar
  11. Corden JM, Millington WM (2001) The long-term trends and seasonal variation of the aeroallergen Alternaria in Derby, UK. Aerobiologia 17:127–136. CrossRefGoogle Scholar
  12. 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. CrossRefGoogle Scholar
  13. 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. CrossRefGoogle Scholar
  14. Damialis A, Gioulekas D (2006) Airborne allergenic fungal spores and meteorological factors in Greece: forecasting possibilities. Grana 45:122–129. CrossRefGoogle Scholar
  15. 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. CrossRefGoogle Scholar
  16. 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. CrossRefGoogle Scholar
  17. 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. CrossRefGoogle Scholar
  18. 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. CrossRefGoogle Scholar
  19. Fitt BDL, McCartney HA, Walklate PJ (1989) The role of rain in dispersal of pathogen inoculum. Annu Rev Phytopathol 27:241–270. CrossRefGoogle Scholar
  20. Frankland AW, Davies RR (1965) Allergie aux spores de moisissures en Angleterre. Poumon Coeur 21:11–23Google Scholar
  21. Galán C, Cariñanos P, Alcázar P, Dominguez E (2007) Manual de calidad y gestión de la Red Española de Aerobiología. Universidad de Córdoba, CordobaGoogle Scholar
  22. 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. CrossRefGoogle Scholar
  23. Gianni C, Cerri A, Crosti C (1997) Ungual phaeohyphomycosis caused by Alternaria alternata. Mycoses 40:219–221. CrossRefGoogle Scholar
  24. Green BJ, Tovey ER, Sercombe JK, Blachere FM, Beezhold DH, Schmechel D (2006) Airborne fungal fragments and allergenicity. Med Mycol 44:S245–S255. CrossRefGoogle Scholar
  25. Grinn-Gofroń A, Bosiacka B (2015) Effects of meteorological factors on the composition of selected fungal spores in the air. Aerobiologia 31:63–72. CrossRefGoogle Scholar
  26. 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. CrossRefGoogle Scholar
  27. 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. CrossRefGoogle Scholar
  28. Grinn-Gofroń A, Strzelczak A (2013) Changes in concentration of Alternaria and Cladosporium spores during summer storms. Int J Biometeorol 57:759–768. CrossRefGoogle Scholar
  29. 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. CrossRefGoogle Scholar
  30. 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. CrossRefGoogle Scholar
  31. Hirst JM (1952) An automatic volumetric spore trap. Ann Appl Biol 39:257–265. CrossRefGoogle Scholar
  32. 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. CrossRefGoogle Scholar
  33. 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 EEUUGoogle Scholar
  34. 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. CrossRefGoogle Scholar
  35. 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 18:88–98Google Scholar
  36. Kasprzyk I (2008) Aeromycology–main research fields of interest during the last 25 years. Ann Agric Environ Med 15(1):1–7Google Scholar
  37. 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. CrossRefGoogle Scholar
  38. Kirk PM, Cannon PF, Minter DW, Stalpers JA (2008) Dictionary of the Fungi, 10th edn. CABI, WallingfordGoogle Scholar
  39. 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. CrossRefGoogle Scholar
  40. Kurkela T (1997) The number of Cladosporium conidia in the air in different weather conditions. Grana 36:54–61. CrossRefGoogle Scholar
  41. Kurup VP, Shen H-D, Vijay H (2002) Immunobiology of fungal allergens. Int Arch Allergy Immunol 129:181–188. CrossRefGoogle Scholar
  42. 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. CrossRefGoogle Scholar
  43. 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. CrossRefGoogle Scholar
  44. 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. CrossRefGoogle Scholar
  45. Machin, D., Campbell, M.J., Walters, S.J., 2007. Medical statisticsGoogle Scholar
  46. 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. CrossRefGoogle Scholar
  47. Myers RH (1990) Classical and modern regression with applications. Duxbury Press Belmont, CAGoogle Scholar
  48. Ogórek R, Lejman R, Pusz W, Miłluch A, Miodyńska P (2012) Characteristics and taxonomy of Cladosporium fungi. Mikol Lek 19:80–85Google Scholar
  49. 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):151–164CrossRefGoogle Scholar
  50. Oliveira M, Ribeiro H, Delgado J, Abreu I (2009a) Aeromycological profile of indoor and outdoor environments. J Environ Monit 11:1360–1367. CrossRefGoogle Scholar
  51. 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. CrossRefGoogle Scholar
  52. 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 26:5–14Google Scholar
  53. 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 11:303–307Google Scholar
  54. Petraitis PS, Dunham AE, Niewiarowski PH (1996) Inferring multiple causality: the limitations of path analysis. Funct Ecol 10:421–431CrossRefGoogle Scholar
  55. 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. CrossRefGoogle Scholar
  56. 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. CrossRefGoogle Scholar
  57. Revankar SG, Sutton DA (2010) Melanized fungi in human disease. Clin Microbiol Rev 23:884–928. CrossRefGoogle Scholar
  58. 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 16:53–61Google Scholar
  59. Rodríguez-Rajo FJ, Iglesias I, Jato V (2005) Variation assessment of airborne Alternaria and Cladosporium spores at different bioclimatical conditions. Mycol Res 109:497–507CrossRefGoogle Scholar
  60. 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 13:217–229Google Scholar
  61. Romano C, Bilenchi R, Alessandrini C, Miracco C (1999) Case Report. Cutaneous phaeohyphomycosis caused by Cladosporium oxysporum. Mycoses 42:111–115. CrossRefGoogle Scholar
  62. Sanchez H, Bush RK (2001) A review of Alternaria alternata sensitivity. Rev Iberoam Micol 18:56–59Google Scholar
  63. Sindt C, Besancenot J-P, Thibaudon M (2016) Airborne Cladosporium fungal spores and climate change in France. Aerobiologia 32:53–68. CrossRefGoogle Scholar
  64. 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, MadridGoogle Scholar
  65. 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. CrossRefGoogle Scholar
  66. Stępalska D, Wołek J (2005) Variation in fungal spore concentrations of selected taxa associated. Aerobiologia 21:43–52. CrossRefGoogle Scholar
  67. Suits DB (1984) Dummy variables: mechanics V. Interpretation. Rev Econ Stat 66:177–180. CrossRefGoogle Scholar
  68. 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. CrossRefGoogle Scholar
  69. 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. CrossRefGoogle Scholar
  70. Thomma BPHJ (2003) Alternaria spp.: from general saprophyte to specific parasite. Mol Plant Pathol 4:225–236. CrossRefGoogle Scholar
  71. Troutt C, Levetin E (2001) Correlation of spring spore concentrations and meteorological conditions in Tulsa, Oklahoma. Int J Biometeorol 45:64–74. CrossRefGoogle Scholar
  72. 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. CrossRefGoogle Scholar
  73. 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. CrossRefGoogle Scholar
  74. Vieira MR, Milheiro A, Pacheco FA (2001) Phaeohyphomycosis due to Cladosporium cladosporioides. Med Mycol 39:135–137. CrossRefGoogle Scholar
  75. 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. CrossRefGoogle Scholar

Copyright information

© ISB 2019

Authors and Affiliations

  1. 1.Department of Environmental Engineering, Engineering FacultyUniversidad Tecnológica de BolívarCartagenaColombia
  2. 2.Institut de Ciència i Tecnologia Ambientals (ICTA)Universitat Autònoma de BarcelonaBarcelonaSpain
  3. 3.Department of Animal Biology, Plant Biology and EcologyUniversitat Autònoma de BarcelonaCerdanyola del VallèsSpain
  4. 4.Department of Managerial Decision SciencesIESE Business SchoolBarcelonaSpain

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