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Review

Impact of Fungal Spores on Asthma Prevalence and Hospitalization

1
NeuroAllergy Research Laboratory (NARL), School of Life and Environmental Sciences, Faculty of Science, Engineering and Built Environment, Deakin University, 221 Burwood Highway, Burwood, VIC 3125, Australia
2
Deakin AIRwatch Pollen and Spore Counting and Forecasting Facility, Deakin University, Burwood, VIC 3125, Australia
3
Institute for Mental and Physical Health and Clinical Translation (IMPACT), Deakin University, 75 Pigdons Road, Waurn Ponds, VIC 3216, Australia
4
NeuroAllergy Research Laboratory (NARL), School of Life and Environmental Sciences, Faculty of Science, Engineering and Built Environment, Deakin University, 75 Pigdons Road, Waurn Ponds, VIC 3216, Australia
5
COVID-19 Response, Department of Health, 50 Lonsdale Street, Melbourne, VIC 3000, Australia
6
School of Life and Environmental Sciences, Faculty of Science, Engineering and Built Environment, Deakin University, 221 Burwood Highway, Burwood, VIC 3125, Australia
7
Centre for Integrative Ecology, School of Life and Environmental Sciences, Faculty of Science, Engineering and Built Environment, Deakin University, 221 Burwood Highway, Burwood, VIC 3125, Australia
*
Author to whom correspondence should be addressed.
Int. J. Mol. Sci. 2022, 23(8), 4313; https://doi.org/10.3390/ijms23084313
Received: 8 March 2022 / Revised: 8 April 2022 / Accepted: 11 April 2022 / Published: 13 April 2022
(This article belongs to the Section Molecular Immunology)

Abstract

:
Despite making up a significant proportion of airborne allergens, the relationship between fungal spores and asthma is not fully explored. Only 80 taxa of fungi have so far been observed to exacerbate respiratory presentations, with Cladosporium spp., Aspergillus spp., Penicillium spp., and Alternaria spp. found to comprise the predominant allergenic airborne spores. Fungal spores have been found in indoor environments, such as hospitals and housing due to poor ventilation. Meanwhile, outdoor fungal spores exhibit greater diversity, and higher abundance and have been associated with hospitalizations from acute asthma presentations. In addition, fungal spores may be the underlying, and perhaps the “missing link”, factor influencing the heightened rate of asthma presentations during epidemic thunderstorm asthma events. To improve our knowledge gap on fungal spores, airborne allergen monitoring must be improved to include not only dominant allergenic fungi but also provide real-time data to accurately and quickly warn the general public. Such data will help prevent future asthma exacerbations and thus save lives. In this review, we examine the health risks of prominent allergenic fungal taxa, the factors influencing spore dispersal and distribution, and why improvements should be made to current sampling methods for public health and wellbeing.

1. Introduction

Approximately one in five individuals suffer from allergic rhinitis worldwide, with prevalence increasing in middle-aged years [1]. It is characterized by symptoms presenting after exposure to airborne allergens. Up to 40% of individuals with allergic rhinitis are also diagnosed with asthma, which can bring about aggravated respiratory symptoms following exposure [2]. Under extreme conditions, exposure could provoke acute asthma exacerbations and lead to hospitalization, most notably during thunderstorm asthma events [3]. While making up a large proportion of airborne allergens, fungal spores have until recently been inadequately studied compared to other aeroallergens like pollen [4]. While it is suggested that at least 5 million unique fungal species exist [5], only 80 taxa have been recognized to date regarding their allergenic potential [6]. Airborne spore diversity varies depending on local meteorological and geographical factors but genera commonly attributed to allergies such as Alternaria spp., Aspergillus spp., Cladosporium spp., and Penicillium spp. are rampant [7,8]. Atmospheric fungal spore concentrations have been observed exceeding pollen counts by 1000 times or more [9,10], reaching as high as 50,000 spores per m3 of air [11]. In addition, fungal spore exposure can last for months as the fungal spore season lasts twice the duration of the pollen season [10], leading to high patient susceptibility for a more significant proportion of the year [12].

2. Fungal Spore Morphology

Compared to pollen, a high degree of diversity can be observed in the morphology of fungal spores (Figure 1). This diversity can be observed even within the genera level and vary depending on geographical features and environmental conditions [13], such as marine vs. high altitude regions, making it challenging to identify some taxa by observation alone. The ability of spores to disperse and remain viable in the atmosphere is mainly dependent on their morphology. The shape of allergenic fungal spores varies, ranging from allantoid (sausage-shaped) to globular [14,15]. Allantoid fungal spores may have a lower risk of being washed out of the air by wind or rain than rounded spores, allowing them to travel further distances [15]. In addition, the surface of fungal spores can vary from smooth to ornamented textures [14] and, like allantoid-shaped spores, ornamentation provides resistance to getting washed out and aids long-distance dispersal [16]. Furthermore, thick-walled spores are resistant to drying out while pigmented spores are resistant to solar radiation [17]. These adaptations also allow fungal spores to remain in the air for extended periods of time.
Fungal spores usually do not exceed 20 µm in diameter, primarily ranging from 3 to 8 µm [14]. Smaller fungal spores can travel greater distances than larger spores [18]. Due to their small size, most allergenic fungal spores can penetrate deep into the lower airways of sensitized individuals [19], similar to sub-pollen particles from rupturing pollen grains [20]. In addition, fungal spores classed as “thermotolerant” thrive at body temperature. Spores have been found submerged and growing in the aqueous lining of the lower respiratory tract and the lungs’ alveoli [21], which can lead to chronic allergic response and infection [22]. Inhalation and deep penetration of fungal spores can invoke severe allergic or asthmatic symptoms.

3. Fungal Sensitization

Fungal sensitization is a potential risk factor for allergic rhinitis and asthma and may contribute to the development of acute respiratory issues [23,24]. The prevalence of fungal allergies is estimated to be 3–10% worldwide [25,26]. Prominent allergenic fungi have been reported to provoke allergic responses in 19–45% of allergic patients and 80% of asthmatic patients from skin tests [27,28,29] and increase the duration of asthmatic symptoms [30]. Atopic workers regularly exposed to fungus and mold spores experience frequent rhinitis and asthma symptoms [31]. About 32.5% of farmers and 16.2% of bakers with occupational asthma are hypersensitive to fungal spores [32].
While Basidiomycota contributes to a majority of aerosol spores, Ascomycota, which make up 4% of airborne fungi, have been strongly linked to allergic rhinitis and asthma [33]. Dominant allergenic fungal taxa, in order of frequency, include Cladosporium spp., Aspergillus spp., Penicillium spp., and Alternaria spp. [34,35,36]. These fungal spores have been observed to worsen symptoms in people diagnosed with asthma, especially children [37,38,39,40].
Alternaria spp. is one of the most well studied airborne fungi in terms of allergic potency and is one of the few spores recognized by allergy specialists [41]. While Alternaria spp. are usually present in lower atmospheric concentrations compared to other allergenic airborne spores, they sport the highest rate of sensitization amongst atopic patients, which is estimated to range from 13–17% [29,42,43], and account for 60% of positive skin prick tests gathered from fungal sensitized patients [8]. Individuals sensitized to Alternaria spp. are also likely to be sensitized to one or more other allergenic fungal taxa [43]. This could be explained by cross-reactivity between fungal allergens that share similar proteins [44]. Positive skin tests for Alternaria spp. have been associated with the presence of asthma and allergic rhinitis; sensitization was not significantly linked to rhinitis alone [45]. Sensitization from exposure to Alternaria spp. usually occurs at a young age [46] and can lead to the development of childhood asthma [47], increasing the frequency of inhaler usage [48,49], and influencing the prevalence of current asthma exacerbations [50]. It is estimated that asthma patients sensitive to Alternaria spp. are 20 times more likely to be at risk of respiratory arrest, which can prove fatal [48]. The impact of Alternaria spp. on asthma has been observed in Australia, with sensitized people found at risk of airway inflammation and severe respiratory presentations from exposure [51]. In addition, Alternaria spp. sensitization has been observed in 13% of hospitalized victims from thunderstorm asthma events in Australia [52]. Immunoglobulin-E specific to Alternaria spp. are more prevalent in sensitized young children after exposure [53]. If they suffer from atopic conditions, it could make them highly vulnerable to exposure to allergenic fungal spores.

4. Hospitalization from Fungal Spores

Preliminary studies found that asthma-related hospital admissions and deaths increased on days with high fungal spore concentrations [4,54]. It was determined that the concentration of specific allergenic fungi, rather than the overall spore concentration, was strongly associated with causing severe respiratory presentations in sensitized populations (Table 1) [55]. High concentrations of Alternaria spp. and Aspergillus spp. have been linked to increased hospital admissions for acute asthma exacerbations [56,57] and patients frequently exposed to Alternaria spp. were at higher risk of being hospitalized [42].
ICU patients admitted for severe asthma are 20% more likely to be sensitive to at least one fungal allergen than non-ICU patients [58]. For instance, penicillin allergy is reported in 10–20% of hospitalized patients, limiting them to more expensive and less effective antibiotic treatments [59,60]. Patients admitted multiple times to the hospital for asthma are up to 4 times more likely to test positive for fungal sensitivity than patients admitted once or never [61]. In addition, patients admitted multiple times are 10 times more likely to have allergic reactions to more than one fungal allergen [61]. Increased exposure and sensitivity to allergenic fungal spores coincide with the severity of asthma presentations [62,63]. While studies have found that fungal spores could have a more significant impact on hospitalizations than pollen [64,65], further research is required to determine the accuracy of these statements.
Table 1. Prevalence and clinical symptoms of prominent allergenic fungal spores.
Table 1. Prevalence and clinical symptoms of prominent allergenic fungal spores.
Fungal SporeAllergy
Prevalence
Environmental
Prevalence
Clinical ManifestationsFatal
Alternaria spp.~13% [66]Indoors & Outdoors [67]
  • Allergic Asthma
  • Allergic Rhinitis
  • Allergic Sinusitis [10,44,66,67,68]
Yes (asthma) [69,70]
Aspergillus spp.~2% [66]Indoors [67]
  • Allergic Asthma
  • Allergic Bronchopulmonary Mycoses (ABPM)
  • Allergic Rhinitis
  • Hypersensitivity Pneumonitis
  • Mycotoxicosis [44,66,67,71,72]
Yes (lung disease) [73]
Cladosporium spp.~3% [66]Indoors & Outdoors [67]
  • Allergic Asthma
  • Allergic Rhinitis
  • Hypersensitivity Pneumonitis [44,66,67,74]
No
Penicillium spp.~2% [66]Indoors [67]
  • Allergic Asthma
  • Allergic Rhinitis
  • Mycotoxicosis [44,66,67]
Yes (infection) [75]

5. Indoor vs. Outdoor Prevalence

While fungal spores are measured in large quantities outside, fungal spores are also common in the indoor environment, primarily from mold growth due to ventilation systems aiding dispersion. Dominant indoor molds include Cladosporium spp., Aspergillus spp., and Penicillium spp. [76]. Homes analyzed in New York found that 98% contained Cladosporium spp. molds and 91% contained Penicillium spp. Molds [77]. Approximately one in five hospital departments in Italy reported fungal pollution, with Aspergillus spp. making up 91.8% of airborne fungal spore load and 68.5% of molds [78]. Fungal contamination has also been found in neonatal hospital wards [79] and indoor Penicillium spp. growth has been identified as the cause of wheezing and breathing problems in newborn infants [80]. Higher rates of allergic reactivity in atopic patients have been reported from exposure to indoor allergens than outdoor allergens [81]. In addition, exposure to indoor fungal spores increases the risk of children developing allergies and asthma over time [82]. However, while the abundance of indoor fungi is dependent on outdoor concentrations and seasonal conditions [83], the level and diversity of indoor fungal spores are exceedingly lower than their counterparts observed outside [84,85]. Furthermore, indoor fungal contamination can be effectively managed via mold removal and remediation [86].
Exposure to Alternaria spp. occurs almost always outdoors [10]. Outdoor fungal spores primarily originate from agricultural lands, with variations in climate governing seasonal fluctuations [87]. Sensitization to outdoor fungal spores is more prevalent than sensitization to indoor fungi [88]. Unlike indoor fungi, which have been primarily linked to allergy and infection, fungal spores prevalent outdoors have been reported to cause acute asthma exacerbations [30]. In addition, outdoor spores have been associated with worsening lung function and heightened airway inflammation, especially in asthma patients [89]. Furthermore, an increase in outdoor fungal spore concentrations was linked to a rise in the number of children admitted to hospitals for asthma presentations [90] and deaths caused by asthma [91].

6. Climate, Pollution, and Fungal Spores

Approximately half of the variation in airborne fungal spore counts can be explained by changes in weather [92]. High temperatures can increase the rate of spore production and the impact of climate change could see spore production rates continue to rise [93]. High humidity leads to heightened levels of basidiospores but decreases dry-air spores like Alternaria spp. and Cladosporium spp. [36,40]. Heavy rain has been observed to remove spores from the air, significantly reducing their concentration and the risk of exposure [94].
Temperature, rain, and relative humidity appear to be the more critical factors influencing fungal spore concentration [95]. However, observations of other weather parameters have not produced consistent results. For instance, wind speeds had no noticeable impact on fungal spore concentrations observed in Turkey [96], sampling carried out in Spain found the wind had a negative effect on fungal spore counts [92], while wind speeds observed in Mexico positively influenced spore concentrations [97]. This suggests that other mechanisms must influence fungal spore counts besides climate alone.
Regions with high vehicular and human traffic have been found to contain increased atmospheric concentrations of fungal spores [98]. A high rate of human activities, such as constructions projects, increases environmental disturbances and encourages the dispersal and distribution of airborne fungal spores [99]. In addition, agricultural regions also have significant contributions to spore production. Plant fungal pathogens infect crops to reproduce, with spores continuously distributed via disturbances like wind or farming practices [100].
Urban communities boast higher pollution levels on average, which could also influence spore production and allergenicity. High PM10 levels have been associated with increased airborne fungi [27]. Elevated CO2 concentrations have been shown to increase Alternaria spp. spore production 3-fold [101]. In addition, fungus exposed to heightened CO2 levels released spores that contained double the average number of allergenic proteins [101]. Elevated CO2 can also lower the resistance of crops to fungal invasion, encouraging the spread and growth of plant fungal pathogens like Alternaria spp., which causes early blight [102,103]. However, other pollutants like ozone and NO2 have had inconclusive effects on fungal spore levels and need to be explored further [104].

7. Fungal Spores and Thunderstorm Asthma

While some studies may have found no consistent links between fungal spore counts and single weather parameters, significant correlations have been found when analyzing variations in weather conditions associated with thunderstorms [105]. Different fungal spore taxa have been observed to increase atmospheric concentrations before, during, and after storms [106]. Elevated levels of Alternaria spp. and Cladosporium spp. are associated with higher temperatures, high ozone concentration, and low humidity, which is characteristic of conditions prior to a thunderstorm [6,40,107]. Static charges created from lightning strikes can also encourage the release of spores into the air [108]. An increase in airborne fungal spores during storms could be the mechanism that causes severe respiratory exacerbations resulting from epidemic thunderstorm asthma events [109].
Early thunderstorm epidemics were first attributed solely to pollen, particularly ruptured grass pollen grains [110,111,112]. However, the presence of high airborne allergenic spore counts on days with asthma epidemics was identified decades ago [113], and analyzing past epidemics found correlations between spikes in fungal spore levels and the occurrence of thunderstorms [114]. The potential role of fungal spores in epidemic thunderstorm asthma has since been more thoroughly investigated. Fungal spore counts have been observed to double on days with storms as rates of asthma admissions increased [109]. Specifically, high concentrations of Alternaria spp. were associated with a rise in asthma presentations across the UK following a thunderstorm, with sensitivity to Alternaria spp. increasing an individual’s risk of suffering from thunderstorm-related asthma exacerbations by 900% [115]. High Cladosporium spp. levels were also observed to increase emergency department admissions for asthma, which were associated with a higher occurrence of thunderstorms [40]. In addition, ruptured Alternaria spp. spores, which are associated with severe asthma presentations, have been collected during thunderstorms [116].

8. Airborne Allergen Sampling Methods

Researchers frequently use sampling traps to collect airborne allergens from internal or external environments. At least 68% of pollen and spore traps currently used worldwide are Hirst-type [117,118]. These sampling traps, first developed in 1952, operate by taking in air volumetrically at 10 L/min and depositing airborne particulates on adhesive-removable surfaces such as tape or microscope slides [119]. The Burkard pollen and spore trap (Figure 2), for instance, is a commonly used Hirst-type sampling device [106] that has been demonstrated to yield high counts of pollen grains and fungal spores and is a reliable method for assessing the atmospheric composition of aeroallergens [120,121].
These traditional sampling traps do have limitations. For instance, sampling machines alone cannot distinguish between local fungal spores and spores dispersed from long distances. Researchers have recently trialed genetically analyzing airborne spores to improve knowledge on local airborne spore diversity, which a sampling trap alone cannot achieve [122]. Similar techniques could be employed at sampling stations across various countries to understand local spore diversity and distribution better. In addition, some Hirst-type sampling traps are less efficient at trapping particulates smaller than 5 µm. While this doesn’t affect larger spores like Alternaria spp. and Cladosporium spp., it may impact the sampling of smaller allergenic spores like Aspergillus spp. and Penicillium spp. [123,124]. However, compared to commercially available spore trap services, Hirst-type traps are currently the most appropriate and widely-used method for obtaining fungal spore data [125]. Furthermore, most sampling machines are designed to collect airborne particles over a long period of time, with the Burkard required to be continuously operating for 24 h to 7 days [126]. While this method can provide researchers with a vast amount of uninterrupted data, the delay caused by these long collection times means the public is not provided with real-time information about the current level of airborne allergens. Developing a sampling regime with shorter collection intervals or with the ability to identify pollen or spores automatically would be a significant improvement over traditional sampling traps. Real-time sampling would allow researchers to monitor current atmospheric aeroallergen concentrations in ways that are overlooked or misjudged by Hirst-type traps [127]. Automatic functional pollen counters have been recently found to be effective in regions with low airborne allergen diversity [128], with some models outperforming traditional samplers [127]. However, this technology is still very new and requires further work to fix critical issues such as low accuracy and the high rate of false positives (e.g., non-pollen identified as pollen) [129,130]. With continued investment, automated systems could be adopted for future aeroallergen monitoring.

9. Conclusions

Spores pose a significant risk to respiratory health and should be taken more seriously for their allergenic potential. Fungal allergens, both indoors and outdoors, are a common cause of rhinitis and asthma exacerbations and are just as potent as pollen. Limiting the exposure of vulnerable populations to allergenic fungal spores is crucial to preventing severe respiratory exacerbations. Thus, more attention needs to be put towards monitoring seasonal fungal spore concentrations. Updating our daily allergen monitoring systems to include allergenic spores will be necessary to accurately detect airborne allergen levels and help develop warning systems to protect the public during thunderstorm-related asthma epidemics. In addition, more sensitive equipment, potentially with real-time automatic sampling, should be developed to improve current monitoring methods and our ability to collect and identify allergenic fungal spores.

Author Contributions

K.M.H.; writing—original draft preparation, D.P.; writing—review and editing, A.A.J.T.; writing—review and editing, M.R.E.S.; writing—review and editing, C.S.; writing—review and editing. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Shakurnia, A.H.; Assarehzadegan, M.A.; Amini, A.; Shakerinejad, G. Prevalence of Fungal Allergens in Respiratory Allergic Patients in Ahvaz City, Southwest Iran. Jundishapur J. Microbiol. 2013, 6, e4864. [Google Scholar] [CrossRef][Green Version]
  2. Khan, D.A. Allergic rhinitis and asthma: Epidemiology and common pathophysiology. Allergy Asthma Proc. 2014, 35, 357–361. [Google Scholar] [CrossRef] [PubMed]
  3. Thien, F. Melbourne epidemic thunderstorm asthma event 2016: Lessons learnt from the perfect storm. Respirology 2018, 23, 976–977. [Google Scholar] [CrossRef] [PubMed]
  4. Jenkins, P.F.; Mullins, J.K.; Davies, B.H.; Williams, D.A. The possible role of aero-allergens in the epidemic of asthma deaths. Clin. Allergy 1981, 11, 611–620. [Google Scholar] [CrossRef]
  5. Blackwell, M. The fungi: 1, 2, 3… 5.1 million species? Am. J. Bot. 2011, 98, 426–438. [Google Scholar] [CrossRef]
  6. Oliveira, M.; Delgado, L.; Ribeiro, H.; Abreu, I. Fungal spores from Pleosporales in the atmosphere of urban and rural locations in Portugal. J. Environ. Monit. 2010, 12, 1187–1194. [Google Scholar] [CrossRef]
  7. Fukutomi, Y.; Taniguchi, M. Sensitization to fungal allergens: Resolved and unresolved issues. Allergol. Int. 2015, 64, 321–331. [Google Scholar] [CrossRef][Green Version]
  8. Sánchez, P.; Vélez-del-Burgo, A.; Suñén, E.; Martínez, J.; Postigo, I. Fungal Allergen and Mold Allergy Diagnosis: Role and Relevance of Alternaria alternata Alt a 1 Protein Family. J. Fungi 2022, 8, 277. [Google Scholar] [CrossRef]
  9. Ianovici, N.; Maria, C.; Radutoiu, M.N.; Hanis, A.; Tudorica, D. Variation in Airborne Fungal Spore Concentrations in Four Different Microclimate Regions in Romania. Not. Bot. Horti Agrobot. Cluj-Napoca 2013, 41, 450. [Google Scholar] [CrossRef][Green Version]
  10. Bush, R.K.; Prochnau, J.J. Alternaria-induced asthma. J. Allergy Clin. Immunol. 2004, 113, 227–234. [Google Scholar] [CrossRef]
  11. Pashley, C.H.; Fairs, A.; Free, R.C.; Wardlaw, A.J. DNA analysis of outdoor air reveals a high degree of fungal diversity, temporal variability, and genera not seen by spore morphology. Fungal Biol. 2012, 116, 214–224. [Google Scholar] [CrossRef]
  12. Guilbert, A.; Simons, K.; Hoebeke, L.; Packeu, A.; Hendrickx, M.; De Cremer, K.; Buyl, R.; Coomans, D.; Van Nieuwenhuyse, A. Short-Term Effect of Pollen and Spore Exposure on Allergy Morbidity in the Brussels-Capital Region. Ecohealth 2016, 13, 303–315. [Google Scholar] [CrossRef] [PubMed][Green Version]
  13. Valsan, A.E.; Priyamvada, H.; Ravikrishna, R.; Després, V.R.; Biju, C.V.; Sahu, L.K.; Kumar, A.; Verma, R.S.; Philip, L.; Gunthe, S.S. Morphological characteristics of bioaerosols from contrasting locations in southern tropical India—A case study. Atmos. Environ. 2015, 122, 321–331. [Google Scholar] [CrossRef]
  14. Priyamvada, H.; Raj Kamal, S.; Akila, M.; Ravikrishna, R.; Rama Shanker, V.; Gunthe, S.S. Seasonal variation of the dominant allergenic fungal aerosols—One year study from southern Indian region. Sci. Rep. 2017, 7, 11171. [Google Scholar] [CrossRef] [PubMed][Green Version]
  15. Calhim, S.; Halme, P.; Petersen, J.H.; Læssøe, T.; Bässler, C.; Heilmann-Clausen, J. Fungal spore diversity reflects substrate-specific deposition challenges. Sci. Rep. 2018, 8, 5356. [Google Scholar] [CrossRef] [PubMed][Green Version]
  16. Gunasekaran, S. A Survey of Spore Ornamentation in Ectomycorrhizal Fungi—Is Ornamentation an Adaptation for Short Distance Dispersal? New York 2012, 5, 1–4. [Google Scholar]
  17. Priyamvada, H.; Akila, M.; Singh, R.K.; Ravikrishna, R.; Verma, R.S.; Philip, L.; Marathe, R.R.; Sahu, L.K.; Sudheer, K.P.; Gunthe, S.S. Terrestrial Macrofungal Diversity from the Tropical Dry Evergreen Biome of Southern India and Its Potential Role in Aerobiology. PLoS ONE 2017, 12, e0169333. [Google Scholar] [CrossRef]
  18. Norros, V.; Rannik, U.; Hussein, T.; Petäjä, T.; Vesala, T.; Ovaskainen, O. Do small spores disperse further than large spores? Ecology 2014, 95, 1612–1621. [Google Scholar] [CrossRef][Green Version]
  19. Zukiewicz-Sobczak, W.A. The role of fungi in allergic diseases. Postepy Dermatol. Alergol. 2013, 30, 42–45. [Google Scholar] [CrossRef][Green Version]
  20. Suphioglu, C.; Singh, M.B.; Taylor, P.; Bellomo, R.; Holmes, P.; Puy, R.; Knox, R.B. Mechanism of grass-pollen-induced asthma. Lancet 1992, 339, 569–572. [Google Scholar] [CrossRef]
  21. Geiser, M.; Leupin, N.; Maye, I.; Hof, V.I.; Gehr, P. Interaction of fungal spores with the lungs: Distribution and retention of inhaled puffball (Calvatia excipuliformis) spores. J. Allergy Clin. Immunol. 2000, 106, 92–100. [Google Scholar] [CrossRef] [PubMed]
  22. Pashley, C.H.; Wardlaw, A.J. Allergic fungal airways disease (AFAD): An under-recognised asthma endotype. Mycopathologia 2021, 186, 609–622. [Google Scholar] [CrossRef] [PubMed]
  23. Tischer, C.G.; Hohmann, C.; Thiering, E.; Herbarth, O.; Müller, A.; Henderson, J.; Granell, R.; Fantini, M.P.; Luciano, L.; Bergström, A.; et al. Meta-analysis of mould and dampness exposure on asthma and allergy in eight European birth cohorts: An ENRIECO initiative. Allergy 2011, 66, 1570–1579. [Google Scholar] [CrossRef] [PubMed]
  24. Sharpe, R.A.; Bearman, N.; Thornton, C.R.; Husk, K.; Osborne, N.J. Indoor fungal diversity and asthma: A meta-analysis and systematic review of risk factors. J. Allergy Clin. Immunol. 2015, 135, 110–122. [Google Scholar] [CrossRef]
  25. Trubiano, J.A.; Cairns, K.A.; Evans, J.A.; Ding, A.; Nguyen, T.; Dooley, M.J.; Cheng, A.C. The prevalence and impact of antimicrobial allergies and adverse drug reactions at an Australian tertiary centre. BMC Infect. Dis. 2015, 15, 572. [Google Scholar] [CrossRef][Green Version]
  26. Salo, P.M.; Arbes, S.J., Jr.; Jaramillo, R.; Calatroni, A.; Weir, C.H.; Sever, M.L.; Hoppin, J.A.; Rose, K.M.; Liu, A.H.; Gergen, P.J.; et al. Prevalence of allergic sensitization in the United States: Results from the National Health and Nutrition Examination Survey (NHANES) 2005–2006. J. Allergy Clin. Immunol. 2014, 134, 350–359. [Google Scholar] [CrossRef][Green Version]
  27. Roy, S.; Chakraborty, A.; Maitra, S.; Bhattacharya, K. Monitoring of airborne fungal spore load in relation to meteorological factors, air pollutants and allergic symptoms in Farakka, an unexplored biozone of eastern India. Environ. Monit. Assess. 2017, 189, 370. [Google Scholar] [CrossRef]
  28. Mari, A.; Schneider, P.; Wally, V.; Breitenbach, M.; Simon-Nobbe, B. Sensitization to fungi: Epidemiology, comparative skin tests, and IgE reactivity of fungal extracts. Clin. Exp. Allergy 2003, 33, 1429–1438. [Google Scholar] [CrossRef]
  29. Arbes, S.J., Jr.; Gergen, P.J.; Elliott, L.; Zeldin, D.C. Prevalences of positive skin test responses to 10 common allergens in the US population: Results from the third National Health and Nutrition Examination Survey. J. Allergy Clin. Immunol. 2005, 116, 377–383. [Google Scholar] [CrossRef]
  30. Pongracic, J.A.; O’Connor, G.T.; Muilenberg, M.L.; Vaughn, B.; Gold, D.R.; Kattan, M.; Morgan, W.J.; Gruchalla, R.S.; Smartt, E.; Mitchell, H.E. Differential effects of outdoor versus indoor fungal spores on asthma morbidity in inner-city children. J. Allergy Clin. Immunol. 2010, 125, 593–599. [Google Scholar] [CrossRef][Green Version]
  31. Klarić, M.; Varnai, V.M.; Calušić, A.L.; Macan, J. Occupational exposure to airborne fungi in two Croatian sawmills and atopy in exposed workers. Ann. Agric. Environ. Med. 2012, 19, 213–219. [Google Scholar] [PubMed]
  32. Wiszniewska, M.; Tymoszuk, D.; Nowakowska-ŚWirta, E.; PaŁCzyŃSki, C.; Walusiak-Skorupa, J. Mould Sensitisation among Bakers and Farmers with Work-related Respiratory Symptoms. Ind. Health 2013, 51, 275–284. [Google Scholar] [CrossRef] [PubMed][Green Version]
  33. Patel, T.Y.; Buttner, M.; Rivas, D.; Cross, C.; Bazylinski, D.A.; Seggev, J. Variation in airborne fungal spore concentrations among five monitoring locations in a desert urban environment. Environ. Monit. Assess. 2018, 190, 634. [Google Scholar] [CrossRef] [PubMed][Green Version]
  34. Ghiasian, S.A.; Maghsood, A.H.; Aghamirian, M.R. Aeromycological analysis of allergenic airborne fungi in Qazvin, Iran. Curr. Med. Mycol. 2016, 2, 5–9. [Google Scholar] [CrossRef] [PubMed][Green Version]
  35. de Ana, S.G.; Torres-Rodríguez, J.M.; Ramírez, E.A.; García, S.M.; Belmonte-Soler, J. Seasonal distribution of Alternaria, Aspergillus, Cladosporium and Penicillium species isolated in homes of fungal allergic patients. J. Investig. Allergol. Clin. Immunol. 2006, 16, 357–363. [Google Scholar] [PubMed]
  36. Oliveira, M.; Ribeiro, H.; Delgado, L.; Fonseca, J.; Castel-Branco, M.G.; Abreu, I. Outdoor allergenic fungal spores: Comparison between an urban and a rural area in northern Portugal. J. Investig. Allergol. Clin. Immunol. 2010, 20, 117–128. [Google Scholar] [PubMed]
  37. Baxi, S.N.; Sheehan, W.J.; Sordillo, J.E.; Muilenberg, M.L.; Rogers, C.A.; Gaffin, J.M.; Permaul, P.; Lai, P.S.; Louisias, M.; Petty, C.R.; et al. Association between fungal spore exposure in inner-city schools and asthma morbidity. Ann. Allergy Asthma Immunol. 2019, 122, 610–615. [Google Scholar] [CrossRef]
  38. Chen, C.H.; Chao, H.J.; Chan, C.C.; Chen, B.Y.; Guo, Y.L. Current asthma in schoolchildren is related to fungal spores in classrooms. Chest 2014, 146, 123–134. [Google Scholar] [CrossRef][Green Version]
  39. Tham, R.; Vicendese, D.; Dharmage, S.C.; Hyndman, R.J.; Newbigin, E.; Lewis, E.; O’Sullivan, M.; Lowe, A.J.; Taylor, P.; Bardin, P.; et al. Associations between outdoor fungal spores and childhood and adolescent asthma hospitalizations. J. Allergy Clin. Immunol. 2017, 139, 1140–1147. [Google Scholar] [CrossRef][Green Version]
  40. Lewis, S.A.; Corden, J.M.; Forster, G.E.; Newlands, M. Combined effects of aerobiological pollutants, chemical pollutants and meteorological conditions on asthma admissions and A & E attendances in Derbyshire UK, 1993–1996. Clin. Exp. Allergy 2000, 30, 1724–1732. [Google Scholar] [CrossRef]
  41. Kasprzyk, I. Co-occurrence of airborne allergenic pollen grains and fungal spores in Rzeszów, Poland (2000–2002). Acta Agrobot. 2008, 61, 65–73. [Google Scholar] [CrossRef][Green Version]
  42. Lehmann, S.; Sprünken, A.; Wagner, N.; Tenbrock, K.; Ott, H. Clinical relevance of IgE-mediated sensitization against the mould Alternaria alternata in children with asthma. Ther. Adv. Respir. Dis. 2017, 11, 30–39. [Google Scholar] [CrossRef] [PubMed][Green Version]
  43. Amado, M.C.; Portnoy, J.M.; Barnes, C. Fungal Cross-Allergenicity In Specific Ige Testing. J. Allergy Clin. Immunol. 2014, 133, AB92. [Google Scholar] [CrossRef]
  44. Denning, D.W.; O’Driscoll, B.R.; Hogaboam, C.M.; Bowyer, P.; Niven, R.M. The link between fungi and severe asthma: A summary of the evidence. Eur. Respir. J. 2006, 27, 615–626. [Google Scholar] [CrossRef][Green Version]
  45. Gergen, P.J.; Turkeltaub, P.C. The association of individual allergen reactivity with respiratory disease in a national sample: Data from the second National Health and Nutrition Examination Survey, 1976–1980 (NHANES II). J. Allergy Clin. Immunol. 1992, 90, 579–588. [Google Scholar] [CrossRef]
  46. Moral, L.; Roig, M.; Garde, J.; Alós, A.; Toral, T.; Fuentes, M.J. Allergen sensitization in children with asthma and rhinitis: Marked variations related to age and microgeographical factors. Allergol. Immunopathol. 2008, 36, 128–133. [Google Scholar] [CrossRef]
  47. Halonen, M.; Stern, D.A.; Wright, A.L.; Taussig, L.M.; Martinez, F.D. Alternaria as a major allergen for asthma in children raised in a desert environment. Am. J. Respir. Crit. Care Med. 1997, 155, 1356–1361. [Google Scholar] [CrossRef]
  48. O’Hollaren, M.T.; Yunginger, J.W.; Offord, K.P.; Somers, M.J.; O’Connell, E.J.; Ballard, D.J.; Sachs, M.I. Exposure to an aeroallergen as a possible precipitating factor in respiratory arrest in young patients with asthma. N. Engl. J. Med. 1991, 324, 359–363. [Google Scholar] [CrossRef]
  49. Delfino, R.J.; Zeiger, R.S.; Seltzer, J.M.; Street, D.H.; Matteucci, R.M.; Anderson, P.R.; Koutrakis, P. The effect of outdoor fungal spore concentrations on daily asthma severity. Environ. Health Perspect. 1997, 105, 622–635. [Google Scholar] [CrossRef]
  50. Salo, P.M.; Arbes, S.J., Jr.; Sever, M.; Jaramillo, R.; Cohn, R.D.; London, S.J.; Zeldin, D.C. Exposure to Alternaria alternata in US homes is associated with asthma symptoms. J. Allergy Clin. Immunol. 2006, 118, 892–898. [Google Scholar] [CrossRef][Green Version]
  51. Downs, S.H.; Mitakakis, T.Z.; Marks, G.B.; Car, N.G.; Belousova, E.G.; Leüppi, J.D.; Xuan, W.; Downie, S.R.; Tobias, A.; Peat, J.K. Clinical importance of Alternaria exposure in children. Am. J. Respir. Crit. Care Med. 2001, 164, 455–459. [Google Scholar] [CrossRef] [PubMed][Green Version]
  52. Harun, N.-S.; Lachapelle, P.; Bowatte, G.; Lodge, C.; Braitberg, G.; Irving, L.; Hinks, T.; Dharmage, S.; Douglass, J. 2016 Thunderstorm-asthma epidemic in Melbourne, Australia: An analysis of patient characteristics associated with hospitalization. Can. J. Respir. Crit. Care Sleep Med. 2021, 5, 276–282. [Google Scholar] [CrossRef]
  53. Nolles, G.; Hoekstra, M.O.; Schouten, J.P.; Gerritsen, J.; Kauffman, H.F. Prevalence of immunoglobulin E for fungi in atopic children. Clin. Exp. Allergy 2001, 31, 1564–1570. [Google Scholar] [CrossRef] [PubMed]
  54. Newson, R.; Strachan, D.; Corden, J.; Millington, W. Fungal and other spore counts as predictors of admissions for asthma in the Trent region. Occup. Environ. Med. 2000, 57, 786–792. [Google Scholar] [CrossRef][Green Version]
  55. Lin, W.R.; Chen, Y.H.; Lee, M.F.; Hsu, L.Y.; Tien, C.J.; Shih, F.M.; Hsiao, S.C.; Wang, P.H. Does Spore Count Matter in Fungal Allergy?: The Role of Allergenic Fungal Species. Allergy Asthma Immunol. Res. 2016, 8, 404–411. [Google Scholar] [CrossRef][Green Version]
  56. Zubairi, A.B.S.; Azam, I.; Awan, S.; Zafar, A.; Imam, A.A. Association of airborne Aspergillus with asthma exacerbation in Southern Pakistan. Asia Pac. Allergy 2014, 4, 91–98. [Google Scholar] [CrossRef][Green Version]
  57. Tham, R.; Dharmage, S.; Taylor, P.; Newbigin, E.; Tang, M.L.K.; Vicendese, D.; Hyndman, R.J.; Abramson, M.J.; Erbas, B. Outdoor fungal spores are associated with child asthma hospitalisations—A case-crossover study. Eur. Respir. J. 2014, 44, 2919. [Google Scholar]
  58. Black, P.N.; Udy, A.A.; Brodie, S.M. Sensitivity to fungal allergens is a risk factor for life-threatening asthma. Allergy 2000, 55, 501–504. [Google Scholar] [CrossRef]
  59. Lee, C.E.; Zembower, T.R.; Fotis, M.A.; Postelnick, M.J.; Greenberger, P.A.; Peterson, L.R.; Noskin, G.A. The incidence of antimicrobial allergies in hospitalized patients: Implications regarding prescribing patterns and emerging bacterial resistance. Arch. Intern. Med. 2000, 160, 2819–2822. [Google Scholar] [CrossRef][Green Version]
  60. Devchand, M.; Trubiano, J.A. Penicillin allergy: A practical approach to assessment and prescribing. Aust. Prescr. 2019, 42, 192–199. [Google Scholar] [CrossRef]
  61. O’Driscoll, B.R.; Hopkinson, L.C.; Denning, D.W. Mold sensitization is common amongst patients with severe asthma requiring multiple hospital admissions. BMC Pulm. Med. 2005, 5, 4. [Google Scholar] [CrossRef][Green Version]
  62. Zureik, M.; Neukirch, C.; Leynaert, B.; Liard, R.; Bousquet, J.; Neukirch, F. Sensitisation to airborne moulds and severity of asthma: Cross sectional study from European Community respiratory health survey. BMJ 2002, 325, 411–414. [Google Scholar] [CrossRef] [PubMed][Green Version]
  63. Neukirch, C.; Henry, C.; Leynaert, B.; Liard, R.; Bousquet, J.; Neukirch, F. Is sensitization to Alternaria alternata a risk factor for severe asthma? A population-based study. J. Allergy Clin. Immunol. 1999, 103, 709–711. [Google Scholar] [CrossRef]
  64. Dales, R.E.; Cakmak, S.; Burnett, R.T.; Judek, S.; Coates, F.; Brook, J.R. Influence of ambient fungal spores on emergency visits for asthma to a regional children’s hospital. Am. J. Respir. Crit. Care Med. 2000, 162, 2087–2090. [Google Scholar] [CrossRef] [PubMed]
  65. Tham, R.; Katelaris, C.H.; Vicendese, D.; Dharmage, S.C.; Lowe, A.J.; Bowatte, G.; Taylor, P.; Burton, P.; Abramson, M.J.; Erbas, B. The role of outdoor fungi on asthma hospital admissions in children and adolescents: A 5-year time stratified case-crossover analysis. Environ. Res. 2017, 154, 42–49. [Google Scholar] [CrossRef] [PubMed]
  66. Simon-Nobbe, B.; Denk, U.; Pöll, V.; Rid, R.; Breitenbach, M. The spectrum of fungal allergy. Int. Arch. Allergy Immunol. 2008, 145, 58–86. [Google Scholar] [CrossRef][Green Version]
  67. Baxi, S.N.; Portnoy, J.M.; Larenas-Linnemann, D.; Phipatanakul, W.; Environmental Allergens, W. Exposure and Health Effects of Fungi on Humans. J. Allergy Clin. Immunol. Pract. 2016, 4, 396–404. [Google Scholar] [CrossRef][Green Version]
  68. Stewart, A.E.; Hunsaker, D.H. Fungus-specific IgG and IgE in allergic fungal rhinosinusitis. Otolaryngol. Head Neck Surg. 2002, 127, 324–332. [Google Scholar] [CrossRef]
  69. Vianello, A.; Caminati, M.; Crivellaro, M.; El Mazloum, R.; Snenghi, R.; Schiappoli, M.; Dama, A.; Rossi, A.; Festi, G.; Marchi, M.R.; et al. Fatal asthma; is it still an epidemic? World Allergy Organ. J. 2016, 9, 42. [Google Scholar] [CrossRef][Green Version]
  70. Plaza, V.; Serrano, J.; Picado, C.; Cosano, J.; Ancochea, J.; de Diego, A.; Martín, J.J.; Sanchís, J. Clinical characteristics of the fatal and near-fatal asthma in Alternaria alternata sensitized patients. Med. Clin. 2003, 121, 721–724. [Google Scholar] [CrossRef]
  71. Eickmeier, O.; Rieber, N.; Eckrich, J.; Hector, A.; Graeppler-Mainka, U.; Hartl, D. Immune response, diagnosis and treatment of allergic bronchopulmonary aspergillosis in cystic fibrosis lung disease. Curr. Pharm. Des. 2013, 19, 3669–3678. [Google Scholar] [CrossRef] [PubMed]
  72. Fracchia, M.S.; El Saleeby, C.M.; Murali, M.R.; Sagar, P.; Mino-Kenudson, M. Case records of the Massachusetts General Hospital. Case 9-2013. A 9-year-old boy with fever, cough, respiratory distress, and chest pain. N. Engl. J. Med. 2013, 368, 1141–1150. [Google Scholar] [CrossRef] [PubMed]
  73. De Lucca, A.J. Harmful fungi in both agriculture and medicine. Rev. Iberoam. Micol. 2007, 24, 3–13. [Google Scholar] [CrossRef]
  74. Watanuki, Z.; Okada, S.; Chiba, S.; Kamei, K.; Suzuki, Y.; Yamada, N. Increased prevalence of high anti-Cladosporium antibody titers in interstitial lung diseases. Tohoku J. Exp. Med. 2012, 226, 287–291. [Google Scholar] [CrossRef][Green Version]
  75. Mok, T.; Koehler, A.P.; Yu, M.Y.; Ellis, D.H.; Johnson, P.J.; Wickham, N.W. Fatal Penicillium citrinum pneumonia with pericarditis in a patient with acute leukemia. J. Clin. Microbiol. 1997, 35, 2654–2656. [Google Scholar] [CrossRef][Green Version]
  76. Cetinkaya, Z.; Fidan, F.; Unlu, M.; Hasenekoglu, I.; Tetik, L.; Demirel, R. Assessment of indoor air fungi in Western-Anatolia, Turkey. Asian Pac. J. Allergy Immunol. 2005, 23, 87–92. [Google Scholar]
  77. Jones, R.; Recer, G.M.; Hwang, S.A.; Lin, S. Association between indoor mold and asthma among children in Buffalo, New York. Indoor Air 2011, 21, 156–164. [Google Scholar] [CrossRef]
  78. Caggiano, G.; Napoli, C.; Coretti, C.; Lovero, G.; Scarafile, G.; De Giglio, O.; Montagna, M.T. Mold contamination in a controlled hospital environment: A 3-year surveillance in southern Italy. BMC Infect. Dis. 2014, 14, 595. [Google Scholar] [CrossRef][Green Version]
  79. Demirel, R.; Sen, B.; Kadaifciler, D.; Yoltas, A.; Okten, S.; Ozkale, E.; Berikten, D.; Samson, R.A.; Haliki Uztan, A.; Yilmaz, N.; et al. Indoor airborne fungal pollution in newborn units in Turkey. Environ. Monit. Assess. 2017, 189, 362. [Google Scholar] [CrossRef]
  80. Rosenbaum, P.F.; Crawford, J.A.; Anagnost, S.E.; Wang, C.J.K.; Hunt, A.; Anbar, R.D.; Hargrave, T.M.; Hall, E.G.; Liu, C.-C.; Abraham, J.L. Indoor airborne fungi and wheeze in the first year of life among a cohort of infants at risk for asthma. J. Expo. Sci. Environ. Epidemiol. 2010, 20, 503–515. [Google Scholar] [CrossRef][Green Version]
  81. Boulet, L.P.; Turcotte, H.; Laprise, C.; Lavertu, C.; Bédard, P.M.; Lavoie, A.; Hébert, J. Comparative degree and type of sensitization to common indoor and outdoor allergens in subjects with allergic rhinitis and/or asthma. Clin. Exp. Allergy 1997, 27, 52–59. [Google Scholar] [CrossRef] [PubMed]
  82. Garrett, M.H.; Rayment, P.R.; Hooper, M.A.; Abramson, M.J.; Hooper, B.M. Indoor airborne fungal spores, house dampness and associations with environmental factors and respiratory health in children. Clin. Exp. Allergy 1998, 28, 459–467. [Google Scholar] [CrossRef] [PubMed]
  83. Sterling, D.A.; Lewis, R.D. Pollen and fungal spores indoor and outdoor of mobile homes. Ann. Allergy Asthma Immunol. 1998, 80, 279–285. [Google Scholar] [CrossRef]
  84. Dacarro, C.; Picco, A.M.; Grisoli, P.; Rodolfi, M. Determination of aerial microbiological contamination in scholastic sports environments. J. Appl. Microbiol. 2003, 95, 904–912. [Google Scholar] [CrossRef][Green Version]
  85. Dassonville, C.; Demattei, C.; Detaint, B.; Barral, S.; Bex-Capelle, V.; Momas, I. Assessment and predictors determination of indoor airborne fungal concentrations in Paris newborn babies’ homes. Environ. Res. 2008, 108, 80–85. [Google Scholar] [CrossRef]
  86. Barnes, C.S.; Dowling, P.; Van Osdol, T.; Portnoy, J. Comparison of indoor fungal spore levels before and after professional home remediation. Ann. Allergy Asthma Immunol. 2007, 98, 262–268. [Google Scholar] [CrossRef]
  87. Skjøth, C.A.; Damialis, A.; Belmonte, J.; De Linares, C.; Fernández-Rodríguez, S.; Grinn-Gofroń, A.; Jędryczka, M.; Kasprzyk, I.; Magyar, D.; Myszkowska, D.; et al. Alternaria spores in the air across Europe: Abundance, seasonality and relationships with climate, meteorology and local environment. Aerobiologia 2016, 32, 3–22. [Google Scholar] [CrossRef][Green Version]
  88. Čelakovská, J.; Bukač, J.; Ettler, K.; Vaneckova, J.; Ettlerova, K.; Krejsek, J. Sensitisation to outdoor and indoor fungi in atopic dermatitis patients and the relation to the occurrence of food allergy to peanuts and walnuts. Mycoses 2018, 61, 698–703. [Google Scholar] [CrossRef]
  89. Tham, R.; Erbas, B.; Dharmage, S.C.; Tang, M.L.K.; Aldakheel, F.; Lodge, C.J.; Thomas, P.S.; Taylor, P.E.; Abramson, M.J.; Lowe, A.J. Outdoor fungal spores and acute respiratory effects in vulnerable individuals. Environ. Res. 2019, 178, 108675. [Google Scholar] [CrossRef]
  90. Tham, R.; Dharmage, S.C.; Taylor, P.E.; Katelaris, C.H.; Vicendese, D.; Abramson, M.J.; Erbas, B. Outdoor fungi and child asthma health service attendances. Pediatr. Allergy Immunol. 2014, 25, 439–449. [Google Scholar] [CrossRef]
  91. Targonski, P.V.; Persky, V.W.; Ramekrishnan, V. Effect of environmental molds on risk of death from asthma during the pollen season. J. Allergy Clin. Immunol. 1995, 95, 955–961. [Google Scholar] [CrossRef]
  92. Sabariego, S.; Bouso, V.; Pérez-Badia, R. Comparative study of airborne Alternaria conidia levels in two cities in Castilla-La Mancha (central Spain), and correlations with weather-related variables. Ann. Agric. Environ. Med. 2012, 19, 227–232. [Google Scholar] [PubMed]
  93. Hollins, P.D.; Kettlewell, P.S.; Atkinson, M.D.; Stephenson, D.B.; Corden, J.M.; Millington, W.M.; Mullins, J. Relationships between airborne fungal spore concentration of Cladosporium and the summer climate at two sites in Britain. Int. J. Biometeorol. 2004, 48, 137–141. [Google Scholar] [CrossRef] [PubMed]
  94. Hirst, J.M. Changes in atmospheric spore content: Diurnal periodicity and the effects of weather. Trans. Br. Mycol. Soc. 1953, 36, 375–393, IN8. [Google Scholar] [CrossRef]
  95. Troutt, C.; Levetin, E. Correlation of spring spore concentrations and meteorological conditions in Tulsa, Oklahoma. Int. J. Biometeorol. 2001, 45, 64–74. [Google Scholar] [CrossRef] [PubMed]
  96. Kalyoncu, F. Relationship between airborne fungal allergens and meteorological factors in Manisa City, Turkey. Environ. Monit. Assess. 2010, 165, 553–558. [Google Scholar] [CrossRef] [PubMed]
  97. Flores, M.E.; Medina, P.G.; Camacho, S.P.; de Jesús Uribe Beltrán, M.; De la Cruz Otero Mdel, C.; Ramírez, I.O.; Hernández, M.E. Fungal spore concentrations in indoor and outdoor air in university libraries, and their variations in response to changes in meteorological variables. Int. J. Environ. Health Res. 2014, 24, 320–340. [Google Scholar] [CrossRef]
  98. Odebode, A.; Adekunle, A.; Stajich, J.; Adeonipekun, P. Airborne fungi spores distribution in various locations in Lagos, Nigeria. Environ. Monit. Assess. 2020, 192, 87. [Google Scholar] [CrossRef][Green Version]
  99. Park, J.H.; Ryu, S.H.; Lee, J.Y.; Kim, H.J.; Kwak, S.H.; Jung, J.; Lee, J.; Sung, H.; Kim, S.-H. Airborne fungal spores and invasive aspergillosis in hematologic units in a tertiary hospital during construction: A prospective cohort study. Antimicrob. Resist. Infect. Control. 2019, 8, 88. [Google Scholar] [CrossRef]
  100. Chambers, K. 2020 Plant Diseases Impacting Oaten hay Production in Australia. Available online: https://agric.wa.gov.au/n/8558 (accessed on 21 October 2021).
  101. Wolf, J.; O’Neill, N.R.; Rogers, C.A.; Muilenberg, M.L.; Ziska, L.H. Elevated atmospheric carbon dioxide concentrations amplify Alternaria alternata sporulation and total antigen production. Environ. Health Perspect. 2010, 118, 1223–1228. [Google Scholar] [CrossRef][Green Version]
  102. Lake, J.A.; Wade, R.N. Plant-pathogen interactions and elevated CO2: Morphological changes in favour of pathogens. J. Exp. Bot. 2009, 60, 3123–3131. [Google Scholar] [CrossRef] [PubMed][Green Version]
  103. Medina-Pérez, G.; Fernández-Luqueño, F.; Campos-Montiel, R.G.; Sánchez-López, K.B.; Afanador-Barajas, L.N.; Prince, L. Chapter 2—Nanotechnology in crop protection: Status and future trends. In Nano-Biopesticides Today and Future Perspectives; Koul, O., Ed.; Academic Press: Cambridge, MA, USA, 2019; pp. 17–45. [Google Scholar]
  104. Ščevková, J.; Hrabovský, M.; Kováč, J.; Rosa, S. Intradiurnal variation of predominant airborne fungal spore biopollutants in the Central European urban environment. Environ. Sci. Pollut. Res. Int. 2019, 26, 34603–34612. [Google Scholar] [CrossRef] [PubMed]
  105. Burch, M.; Levetin, E. Effects of meteorological conditions on spore plumes. Int. J. Biometeorol. 2002, 46, 107–117. [Google Scholar] [CrossRef] [PubMed]
  106. Ščevková, J.; Dušička, J.; Tropeková, M.; Kováč, J. Summer storms and their effects on the spectrum and quantity of airborne bioparticles in Bratislava, Central Europe. Environ. Monit. Assess. 2020, 192, 537. [Google Scholar] [CrossRef] [PubMed]
  107. Grinn-Gofroń, A.; Strzelczak, A. Changes in concentration of Alternaria and Cladosporium spores during summer storms. Int. J. Biometeorol. 2013, 57, 759–768. [Google Scholar] [CrossRef][Green Version]
  108. Leach, C.M. An Electrostatic Theory to Explain Violent Spore Liberation by Drechslera turcica and Other Fungi. Mycologia 1976, 68, 63–86. [Google Scholar] [CrossRef]
  109. Dales, R.E.; Cakmak, S.; Judek, S.; Dann, T.; Coates, F.; Brook, J.R.; Burnett, R.T. The role of fungal spores in thunderstorm asthma. Chest 2003, 123, 745–750. [Google Scholar] [CrossRef][Green Version]
  110. Venables, K.M.; Allitt, U.; Collier, C.G.; Emberlin, J.; Greig, J.B.; Hardaker, P.J.; Highham, J.H.; Laing-Morton, T.; Maynard, R.L.; Murray, V.; et al. Thunderstorm-related asthma—The epidemic of 24/25 June 1994. Clin. Exp. Allergy 1997, 27, 725–736. [Google Scholar] [CrossRef]
  111. Bellomo, R.; Gigliotti, P.; Treloar, A.; Holmes, P.; Suphioglu, C.; Singh, M.B.; Knox, B. Two consecutive thunderstorm associated epidemics of asthma in the city of Melbourne. The possible role of rye grass pollen. Med. J. Aust. 1992, 156, 834–837. [Google Scholar] [CrossRef]
  112. Celenza, A.; Fothergill, J.; Kupek, E.; Shaw, R.J. Thunderstorm associated asthma: A detailed analysis of environmental factors. BMJ 1996, 312, 604–607. [Google Scholar] [CrossRef][Green Version]
  113. Salvaggio, J.; Seabury, J.; Schoenhardt, F.A. New Orleans asthma. V. Relationship between Charity Hospital asthma admission rates, semiquantitative pollen and fungal spore counts, and total particulate aerometric sampling data. J. Allergy Clin. Immunol. 1971, 48, 96–114. [Google Scholar] [CrossRef]
  114. Allitt, U. Airborne Fungal Spores and the Thunderstorm of 24 June 1994. Aerobiologia 2000, 16, 397. [Google Scholar] [CrossRef]
  115. Pulimood, T.B.; Corden, J.M.; Bryden, C.; Sharples, L.; Nasser, S.M. Epidemic asthma and the role of the fungal mold Alternaria alternata. J. Allergy Clin. Immunol. 2007, 120, 610–617. [Google Scholar] [CrossRef] [PubMed]
  116. Rabe, U. Are Fungal Spores Relevant Outdoor Allergens? Laryngorhinootologie 2020, 99, 292–298. [Google Scholar] [CrossRef]
  117. Hirst, J.M. An automatic volumentric spore trap. Ann. Appl. Biol. 1952, 39, 257–265. [Google Scholar] [CrossRef]
  118. Buters, J.T.M.; Antunes, C.; Galveias, A.; Bergmann, K.C.; Thibaudon, M.; Galán, C.; Schmidt-Weber, C.; Oteros, J. Pollen and spore monitoring in the world. Clin. Transl. Allergy 2018, 8, 9. [Google Scholar] [CrossRef]
  119. Levetin, E.; Rogers, C.A.; Hall, S.A. Comparison of pollen sampling with a Burkard Spore Trap and a Tauber Trap in a warm temperate climate. Grana 2000, 39, 294–302. [Google Scholar] [CrossRef]
  120. Crisp, H.C.; Gomez, R.A.; White, K.M.; Quinn, J.M. A side-by-side comparison of Rotorod and Burkard pollen and spore collections. Ann. Allergy Asthma Immunol. 2013, 111, 118–125. [Google Scholar] [CrossRef]
  121. Buttner, M.P.; Stetzenbach, L.D. Monitoring airborne fungal spores in an experimental indoor environment to evaluate sampling methods and the effects of human activity on air sampling. Appl. Environ. Microbiol. 1993, 59, 219–226. [Google Scholar] [CrossRef][Green Version]
  122. Ovaskainen, O.; Abrego, N.; Somervuo, P.; Palorinne, I.; Hardwick, B.; Pitkänen, J.-M.; Andrew, N.R.; Niklaus, P.A.; Schmidt, N.M.; Seibold, S.; et al. Monitoring Fungal Communities With the Global Spore Sampling Project. Front. Ecol. Evol. 2020, 7, 511. [Google Scholar] [CrossRef][Green Version]
  123. Yamamoto, N.; Bibby, K.; Qian, J.; Hospodsky, D.; Rismani-Yazdi, H.; Nazaroff, W.W.; Peccia, J. Particle-size distributions and seasonal diversity of allergenic and pathogenic fungi in outdoor air. ISME J. 2012, 6, 1801–1811. [Google Scholar] [CrossRef] [PubMed][Green Version]
  124. Khattab, A.; Levetin, E. Preliminary studies on the effect of the Burkard alternate orifice on airborne fungal spore concentrations. Aerobiologia 2008, 24, 165–171. [Google Scholar] [CrossRef]
  125. Robertson, L.D.; Brandys, R. A multi-laboratory comparative study of spore trap analyses. Mycologia 2011, 103, 226–231. [Google Scholar] [CrossRef] [PubMed][Green Version]
  126. Peel, R.G.; Kennedy, R.; Smith, M.; Hertel, O. Relative efficiencies of the Burkard 7-Day, Rotorod and Burkard Personal Samplers for Poaceae and Urticaceae pollen under field conditions. Ann. Agric. Environ. Med. 2014, 21, 745–752. [Google Scholar] [CrossRef][Green Version]
  127. Damialis, A.; Kolek, F.; Glaser, M.; Brunner, J.; Traidl-Hoffmann, C. Automatic, Real-Time Pollen Monitoring for Allergic Patients: The Good, the Bad or the Ugly? In Proceedings of the 11th International Congress on Aerobiology. Parma, Italy, 3–7 September 2019. [Google Scholar]
  128. Oteros, J.; Pusch, G.; Weichenmeier, I.; Heimann, U.; Möller, R.; Röseler, S.; Traidl-Hoffmann, C.; Schmidt-Weber, C.; Buters, J.T. Automatic and Online Pollen Monitoring. Int. Arch. Allergy Immunol. 2015, 167, 158–166. [Google Scholar] [CrossRef]
  129. Sauvageat, E.; Zeder, Y.; Auderset, K.; Calpini, B.; Clot, B.; Crouzy, B.; Konzelmann, T.; Lieberherr, G.; Tummon, F.; Vasilatou, K. Real-time pollen monitoring using digital holography. Atmos. Meas. Tech. 2020, 13, 1539–1550. [Google Scholar] [CrossRef][Green Version]
  130. Schiele, J.; Rabe, F.; Schmitt, M.; Glaser, M.; Häring, F.; Brunner, J.O.; Bauer, B.; Schuller, B.; Traidl-Hoffmann, C.; Damialis, A. Automated Classification of Airborne Pollen using Neural Networks. In Proceedings of the 2019 41st Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC), Berlin, Germany, 23–27 July 2019; pp. 4474–4478. [Google Scholar]
Figure 1. Visualization of the diversity in shape, pigmentation, and ornamentation amongst pollen grains (left) and fungal spores (right). Pollen grains commonly feature pores, colpi, or reticulated mesh. In contrast, fungal spores have more diverse shapes and ornamented textures. Image features artistic representations of Pine (Pinaceae) pollen (a), Plantain (Plantago) pollen (b), Olive (Oleaceae) pollen (c), Grass (Poaceae) pollen (d), Leptosphaeria spp. spores (e), Pithomyces spp. spores (f), Pleospora spp. spores (g), Ganoderma spp. spores (h), Coprinus spp. spores (i), Chaetomium spp. spores (j), Alternaria spp. spores (k), and Cladosporium spp. spores (l).
Figure 1. Visualization of the diversity in shape, pigmentation, and ornamentation amongst pollen grains (left) and fungal spores (right). Pollen grains commonly feature pores, colpi, or reticulated mesh. In contrast, fungal spores have more diverse shapes and ornamented textures. Image features artistic representations of Pine (Pinaceae) pollen (a), Plantain (Plantago) pollen (b), Olive (Oleaceae) pollen (c), Grass (Poaceae) pollen (d), Leptosphaeria spp. spores (e), Pithomyces spp. spores (f), Pleospora spp. spores (g), Ganoderma spp. spores (h), Coprinus spp. spores (i), Chaetomium spp. spores (j), Alternaria spp. spores (k), and Cladosporium spp. spores (l).
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Figure 2. Schematic of Hirst-type 24-h Burkard pollen and spore trap (a) and internal microscope slide holder (b).
Figure 2. Schematic of Hirst-type 24-h Burkard pollen and spore trap (a) and internal microscope slide holder (b).
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Hughes, K.M.; Price, D.; Torriero, A.A.J.; Symonds, M.R.E.; Suphioglu, C. Impact of Fungal Spores on Asthma Prevalence and Hospitalization. Int. J. Mol. Sci. 2022, 23, 4313. https://doi.org/10.3390/ijms23084313

AMA Style

Hughes KM, Price D, Torriero AAJ, Symonds MRE, Suphioglu C. Impact of Fungal Spores on Asthma Prevalence and Hospitalization. International Journal of Molecular Sciences. 2022; 23(8):4313. https://doi.org/10.3390/ijms23084313

Chicago/Turabian Style

Hughes, Kira M., Dwan Price, Angel A. J. Torriero, Matthew R. E. Symonds, and Cenk Suphioglu. 2022. "Impact of Fungal Spores on Asthma Prevalence and Hospitalization" International Journal of Molecular Sciences 23, no. 8: 4313. https://doi.org/10.3390/ijms23084313

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