ACTA AGROBOTANICA Vol. 62 (1): 3–8 2009

THE OF Alternaria IN AEROPLANKTON AND ITS RELATIONSHIPS WITH THE METEOROLOGICAL FACTORS

Agnieszka Grinn-Gofroń

Department of Taxonomy and Phytogeography, Faculty of Natural Science University of Szczecin, Wąska 13, 71-415 Szczecin, Poland e-mail: [email protected]

Received: 16.02.2009

Abstract individuals. The characteristic features and size of the Alternaria spores are known to be potent aeroallergens spores determine how deep they may penetrate into the and their concentrations in the air are strongly dependent on respiratory tract, whereby the exact site of allergic re- meteorological factors. There are many articles from different sponse can be determined. Spores larger than 10 μm parts of the world about relationships between Alternaria in diameter are deposited in the nasopharynx causing count and weather parameters. The aim of the study was to re- rhinitis; spores smaller than 5 μm penetrate to the ale- view all available publications about airborne Alternaria spores voli causing alevolitis. Spores <10 μm in size mostly and compare the results in short, useful form. deposit in the bronchi and bronchioles causing (Lacey et al. 1972). Key words: Alternaria, airborne spores, meteorological fac- One of the most important genus belonging tors, statistical correlation to that group is Alternaria. There is a number of very similar, related species which are usually grouped to- gether as Alternaria. The spores are multi-celled. The INTRODUCTION conidiophores are dark, simple, rather short or elon- gate, typically bearing a simple or branched chain of The form-division Fungi Imperfecti or Deu- conidia. The conidia are also dark, multi-septate, both teromycota is an artificial category. Members of this transverse and longitudinal. They vary in width and group were originally combined into a single group length according to species, usually 8 to 75 microme- because they apparently lacked a sexual stage. Fungi ters in length; some species, such as Alternaria longis- Imperfecti are divided into form-classes based upon sima, can be found with a length of up to 500 microm- morphological similarities. The criteria that are typi- eters (0.5 milimeters). cally used are colour, shape, size and septation of the Alternaria, which is both ubiquitous and abun- conidia (whether the spores are unicellular, or made up dant, is both saprophytic and parasitic on plant mate- of multiple cells). Many of the spores of the Fungi Im- rial and is found on rotting vegetation as well as in perfecti have morphologically distinct features so that damp indoor areas, such as bathrooms. The spores are the spores from this group are some of the most easily present in large number throughout the late summer, es- identified. Many are also easily cultured so that more pecially at the harvest time (Hyde and Williams, research has been conducted upon this group of fungi 1946). Geographically, the is distributed world- than many other. Alternaria, Cladosporium, Curvu- wide but is particularly prevalent in dry climates. laria, Drechslera, Epicoccum, Fusarium, Nigrospora Certain fungal spores are known to cause an al- and Stemphylium were listed by Kendrick (1990) lergic response and spores of the genus Alternaria have as the ‘Big Eight’ because of their allergenicity and been known to trigger asthma for over 50 years (Hop- frequency in the air. kins et al. 1939). The risk of asthma-related deaths is The knowledge of the composition of airborne more than doubled when there is a high incidence of spores of a particular area is important in agriculture, mould spores (Targonsky et al. 1995) and Alter- because crop pathogens can be identified to prevent naria is a known risk factor in childhood and young crop epidemics and also because some of them act as adult asthma (O’Hollaren et al. 1991; Tariq et factors for causing respiratory allergy to susceptible al. 1996; Dutkiewicz, 1997). 4 Agnieszka Grinn-Gofroń

Alternaria spores vary in size, but Licorish tion and the maximum temperatures has been found et al. (1985) said it could be safely assumed that even in Szczecin (Grinn-Gofroń , 2008) and has been the larger Alternaria spores could penetrate the lungs reported from other sites in Poland (S t ę palska and causing asthma. If more Alternaria spores are being Woł ek, 2005), United States (Levetin and Dor- released into the air, even though only a small percent- sey, 2006), United Kingdom (Corden and Mil- age of the population is involved, then a considerable lington, 2001) and Spain (Fernández et al. number of patients may have severe asthma attacks 1998). Herrero et al. (1996) studied the relationship during the Alternaria season. between daily concentrations of Alternaria and mete- Literature has a few references to the number orological variables. They found Alternaria to be posi- of spores that are needed to provoke an allergic reac- tively correlated with maximum temperature. tion in susceptible individuals. One estimated thresh- old concentration of Alternaria spores needed to pro- Minimum temperature voke an allergic response is 100 spores ‰ m-3 of air (Gravesen, 1979). Licorish et al. (1985), how- The correlation between Alternaria spore count ever, suggests that the order of 104-107 spores is needed and minimum temperature was not significant in all to be inhaled over 24-h period. Hasnain (1993) sug- available publications. gests that mean daily concentrations of 50 Alternaria spores/m3 are needed to cause sensitization, after which Mean temperature smaller concentrations can cause symtoms. In Poland The content of Alternaria spores in the atmos- Rapiejko et al. (2004) reported that a subject with phere increases when mean temperatures rise; these hypersensitivity to Alternaria allergens experienced results are very similar to those obtained by other au- the symptoms during exposure to a concentration of thors (Infante and Dominquez, 1988 (Cordoba, approximately 80 spores ‰m-3 of air. Spain); Gonzáles Minero et al. 1994 (Spain); Ricci et al. 1995; Méndez et al. 1997 (Spain), who The highest concentrations considered that this factor played a major role in the The monitoring of fungal spores in Poland re- dispersion of Alternaria. Positive, significant correla- vealed the summer as the most favourable season for tions with temperature, similar to those observed in Alternaria occurrence (Gaweł , 1996; S t ę palska Poland, have been reported extensively in other cities et al. 1999; Kasprzyk et al. 2004; Konopiń ska, throughout the world by Palmas and Cosentino, 2004; S t ę palska and Woł ek, 2005; Grinn- 1990 (Sardinia, Italy); Rosas et al. 1990 (Mexico); Gofroń and Strzelczak, 2008). Also in Den- Srivastawa and Wadhwani, 1992 (SE Spain); mark (Larsen and Gravesen, 1991) and Sweden (Fernández-Gonzáles et al. 1993 (Leon, (Hjelmroos, 1993), the highest number of Alter- Spain); Hjelmroos, 1993 (Stockholm, Sweden); M i - naria spores was usually encountered during summer. takakis et al. 1997 (Melbourne, Australia); Pare- In Cordoba (Infante and Dominquez, 1988) des et al. 1997 (Mexico); Munuera Giner et and on Sardinia (Cosentino et al. 1990), a decrease al. 2001 (SE Spain); Troutt and Levetin, 2001 in the Alternaria spore concentration was observed in (Tulsa, United States); Sakiyan and Inceoğ lu, summer. The summer decrease is related to high tem- 2003 (Ankara, Turkey). perature and lack of rain. Maximum concentrations were found in Cordoba to occur in both late spring and Relative humidity autumn (Angulo-Romero et al. 1999). Contrary to these results in Amman (Jordan), maximum Alter- The Alternaria spores count was negatively and naria spore counts were recorded in October, because statistically significantly correlated with relative air of wet, warm, conditions (Shaheen, 1992). In the humidity, however, a positive correlation (increased United States, various surveys have reported Alter- spore count in the air with increased relative humid- naria more frequently than other moulds (except on ity) was noted by S t ę palska and Woł ek (2005) the Pacific Coast where this taxon was found only in Cracow, by Hjelmroos (1993) in Stockholm and sporadically or in reduced numbers (D’Amato and in Ankara (Sakiyan and Inceoğ lu, 2003). The Spieksma, 1995). concentration of Alternaria spores in the suburbs of Mexico City was found by Calderon et al. (1997) Correlations with meteorological factors to be positively correlated with relative humidity on the Maximum temperature previous day. Giner and Garcia (1995) in Murcia (Spain) found that daily concentrations of Alternaria A positive and statistically significant corre- spores were positively correlated with relative humid- lation between the daily Alternaria spore concentra- ity but not significantly. The spores of Alternaria in aeroplankton and its relationships with the meteorological factors 5

Rainfall using a forward stepwise mode, showed a significant negative correlation between Alternaria spore count A significant and negative correlation between and dew point temperature but positive for tempera- the Alternaria spores concentration and daily precipi- ture. They conclude that temperature and dew point tation was noted by S t ę palska and Woł ek in are probably the best predictors for Alternaria, appear- Cracow (2005), Mitakakis et al. (1997) in Austral- ing with positive and negative relationships in all re- ia, Corden and Milington (2001) in the United gressions. Kingdom and Sakiyan and Inceoğ lu, (2003) in Turkey. Herrero et al. (1996) reported a posi- Statistical models tive correlation with rainfall. Giner and Garcia (1995) found that daily concentrations of Alternaria A better understanding of the relative impor- spores were positively correlated with precipitation tance of weather parameters and their interrelation- but not significantly. Gregory and Hirst, (1957) ships would help determine the role of spore dispersal in Rothmasted found high Alternaria spore concentra- in allergies to airborne fungal spores. However, there tions most often in August, in warm, dry spells after are comparatively few advanced forecasting models of a period of wet weather. Based on the available pub- airborne fungal spore circulation (Katial et al. 1997), lications, we have some evidence that although high and most of them usually display low predictability daily Alternaria spore levels occur on dry days, occa- (Angulo-Romero et al. 1999; Mitakakis et sional rainfall results in higher monthly concentrations al. 2001; Stennett and Beggs, 2004). of Alternaria spores than that in a longer dry period. In Herrero et al. (1996) noted a positive signifi- Amman the maximum Alternaria spore counts in the cant correlation for precipitation using two statistical air were noted in warm, wet conditions (Shaheen, analyses: multiple regression and Duncan’s multiple 1992). range test. Lyon et al. (1884), using multiple re- gression analysis, also noted that the maximum and speed minimum temperatures are significantly correlated In Szczecin, which is almost flat, wind speed was with concentrations of Alternaria. Damialis and not significantly correlated with spore concentrations Gioulekas (2006) used the autoregressive pre- (Grinn-Gofroń , 2008). In Stockholm Hjelm- dictive models and observed Alternaria spores were roos (1993) noted that the concentration of Alter- strongly related to air temperature. The interaction ef- naria spores was favoured by relatively strong . fects of rainfall and wind were also considered nec- Similar results occurred in Ankara (Sakiyan and essary for long-term (annual) predictions of airborne Inceoğ l u , 2003). A negative correlation between fungal concentrations. the Alternaria spores count and the wind speed was Spearman’s rank correlation coefficient and observed by Levetin and Dorsey (2006) in Tulsa also multiple regression were used by Stennett and (United States) and by Hasnain, (1993) in Auckland Beggs (2004) in Sydney. The daily mean, minimum (New Zeland). Lopez and Salvaggio (1983) also and maximum temperature and dew point temperature confirmed that high wind speed produced a decreased were most strongly and consistently associated with the atmospheric concentration of Alternaria spores count. concentration of Alternaria spores. The same authors Giner and Garcia (1995) found that daily concen- found positive, but markedly lower and less consistent, trations of Alternaria spores were positively correlated relationships between Alternaria spore concentration with wind speed but not significantly. and rainfall 2 and 3 days previously and relative hu- midity in the previous 1, 2 and 3 days. Pressure Contrary to the results presented above, Hjelmroos, (1993) and Katial et al. (1997) not- Hjelmroos (1993) noted a negative signifi- ed no statistically significant correlation between Al- cant correlation for Cladosporium in Sweden and for ternaria spore count and weather variables and they Alternaria the correlation was not statistically signifi- consider that no statistical model can be proposed for cant. A highly significant negative correlation between Alternaria spore concentrations in relation to climate. air pressure and Alternaria spore concentration was The models created by Grinn-Gofroń and found by Stennett and Beggs (2004) in Sydney, Strzelczak (2008) for relationships between Al- although this occurred only on the same day and with ternaria spore concentrations and meteorological fac- one day lag. tors are based mainly on the artificial neural network (ANN) method. All variables, except maximum wind Dew point temperature speed and precipitation, were important factors in the Troutt and Levetin (2001), in the results overall classification model. In the regression model for of multiple regression analysis which was performed spore seasons, close relationships were noted between 6 Agnieszka Grinn-Gofroń

Alternaria spore concentration, average and maximum F e r n á n d e z D., Va l e n c i a R. M., M o l n a r T., Ve g a A., temperature (on the same day and 3 days previously), Sagues E., 1998. Daily and seasonal variations of Al- humidity (with lag 1) and maximum wind speed 2 days ternaria and Cladosporium airborne spores in Leon previously. The most important variable was humidity (North-West, Spain). Aerobiologia, 14: 215-220. recorded on the same day. Fernández-Gonzáles D., Suárez-Cervera M., That study shows the novel approach to mod- Diaz-Gonzáles T., Valencia-Barrera R. M., elling of time series with short spore seasons and in- 1993. Airborne and spores of León (Spain). Int. dicates that the ANN method gives the possibility of J. Biometeorol. 37: 89-95. forecasting Alternaria spore concentration with high Gaweł J., H a l o t a A., P i s i e w i c z K., K u r z a w a R., accuracy. Radliń s k i J., D o n i e c Z., 1996. 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W ciągu ostatnich kilku lat ukazało się kilka Przy obecnym stanie badań nad relacjami sta- prac z prognostycznymi modelami statystycznymi tystycznymi pomiędzy obecnością (stężeniem) zarod- (Szwecja, Grecja, Polska). ników w powietrzu a czynnikami meteorologicznymi Statystycznie istotne, pozytywne korelacje były warto budować statystyczne modele prognostyczne, notowane dla dobowych temperatur maksymalnych które dają bardziej precyzyjne informacje o badanych i średnich a negatywne dla: wysokości opadów desz- związkach i znacznie upraszczają prognozowanie se- czu, ciśnienia atmosferycznego, temperatury punktu zonów zarodnikowania i konstruowanie kalendarzy rosy i prędkości wiatru. Żaden z autorów nie zano- dla lekarzy alergologów. tował istotnej statystycznie korelacji pomiędzy stę- żeniem zarodników rodzaju Alternaria a temperaturą minimalną.