1. Introduction
Fungal organisms are common in indoor and outdoor air environments. They are known to induce irritation, infection, allergy, asthma, and toxic effects [
1,
2]. Fungi may produce mycotoxins that may cause several diseases in humans and animals. Knowledge of indoor airborne fungi is important, as various fungi could be common in indoor air of occupational and non-occupational buildings.
In the recent years, assessment of buildings for evidence of indoor fungal growth has dramatically increased [
3,
4]. Many studies have focused on fungal concentrations in problematic or moldy contaminated buildings [
5,
6], and few references for normal buildings without mold damage [
7,
8]. Nevalainen
et al. reported that the presence of indoor fungi and air quality problems could still occur in buildings without moisture or mold damage [
9]. Fungal organisms are known to induce irritation, infection, allergy, asthma, and toxic effects [
5,
6].
The concentrations and types of airborne fungi depend on time of day, climatic conditions, geographical location and type of vegetation [
10]. Airborne fungal concentrations in homes and schools ranged between 10
2 and 10
4 CFU/m
3 in warm climates [
11], and averaged 10
2 CFU/m
3 in cold subarctic climates [
12]. Airborne fungal concentrations exceeded 10
4 CFU/m
3 in the moldy homes, and <200 CFU/m
3 in the reference dwellings (without mold growth), with
Penicillium,
Aspergillus,
Cladosporium and
Alternaria being the common genera found [
13]. In Poland, fungal concentrations averaged 60 CFU/m
3 in healthy homes in winter, and >800 CFU/m
3 in moldy homes in summer, with the maximum concentration reaching 17,000 CFU/m
3 [
14]. There is a growing interest in indoor air quality as the concentrations and prevalence of fungi in a particular region help identify the association between residential exposure, clinical diagnosis, and in the prevention of seasonal allergic diseases [
15]. The aim of the present study was to assess concentrations, types and frequency of distributions of indoor and outdoor fungi in the air of urban and rural homes without a suspected or known problem, in order to gain data on home-indoor air quality in Egypt.
4. Discussion
Many studies have been performed to identify the concentrations and types of airborne fungal organisms in buildings all over the world. Almost all studies have focused on problematic buildings; however few reported research non-problematic building or on indoor air quality from Egypt.
In the present study, fungal concentrations were higher in the rural environment and may be a result of outdoor fungal sources, such as “animal shelters, solid-waste, composts, plant debris and vegetation”. The rate of air exchange may be higher in the rural homes where the rate of air ventilation from outdoor to indoor may help increase the indoor fungal concentrations. In milder climates the outdoor fungal organisms are the largest source of indoor concentrations of fungi and the outdoor concentration can routinely exceed of 10
3 CFU/m
3 [
23]. In addition indoor fungi are directly dependent on building type, hygienic rules and ventilation [
24]; life style and residential characteristics [
15,
25], and the rural homes in this study were characterized by higher ventilation rates, larger areas and dusty floors.
Table 5.
The total counts (CFU/m3) for the indoor (In) and outdoor (Out) most prevalent fungal organisms recovered by season.
Table 5.
The total counts (CFU/m3) for the indoor (In) and outdoor (Out) most prevalent fungal organisms recovered by season.
| Urban | Rural |
---|
Winter | Spring | Summer | Autumn | Winter | Spring | Summer | Autumn |
---|
| In | Out | In | Out | In | Out | In | Out | In | Out | In | Out | In | Out | In | Out |
---|
Alternaria | 120 | 135 | 333 | 959 | 737 | 975 | 89 | 30 | 351 | 819 | 4,424 | 6,380 | 1,040 | 880 | 34 | 291 |
Aspergillus spp. | 7,726 | 6,804 | 3,230 | 3,860 | 11,062 | 7,989 | 8,334 | 8,136 | 4,889 | 3,896 | 1,488 | 800 | 6,997 | 5,104 | 5,214 | 3,779 |
Cladosporium | 33 | 65 | 7,707 | 7,145 | 2,096 | 4,150 | 12,190 | 19,086 | 18,603 | 31,689 | 124,268 | 277,714 | 5,912 | 4,148 | 11,611 | 11,117 |
Fusarium | 105 | 104 | 306 | 1,560 | 558 | 288 | 110 | 0 | 689 | 599 | 1,724 | 1,560 | 2,440 | 2,924 | 627 | 639 |
Penicillium | 11,911 | 8,340 | 5,221 | 6,021 | 2,498 | 1,750 | 5,365 | 8,568 | 5,650 | 4,805 | 12,700 | 45,428 | 3,896 | 3,176 | 6,323 | 4,421 |
Yeasts | 119 | 194 | 1,280 | 1,123 | 996 | 884 | 22 | 37 | 910 | 555 | 2,640 | 4,144 | 1,560 | 1,160 | 691 | 316 |
Other | 1,170 | 1,154 | 8,354 | 8,181 | 2,921 | 5,318 | 13,594 | 20,394 | 23,174 | 35,863 | 125,957 | 278,914 | 8,678 | 5,358 | 16,523 | 14,161 |
Total | 21,151 | 16,731 | 18,724 | 21,704 | 18,772 | 17,204 | 27,514 | 37,165 | 35,663 | 46,537 | 148,933 | 337,226 | 24,611 | 18,602 | 29,412 | 23,607 |
Table 6.
Frequency of occurrence (n = 26-urban, n = 17-rural) as percent of homes positive for most prevalent fungal organisms for the indoor (In) and outdoor (Out) by season.
Table 6.
Frequency of occurrence (n = 26-urban, n = 17-rural) as percent of homes positive for most prevalent fungal organisms for the indoor (In) and outdoor (Out) by season.
| Winter | Spring | Summer | Autumn |
---|
Urban | Rural | Urban | Rural | Urban | Rural | Urban | Rural |
---|
In | Out | In | Out | In | Out | In | Out | In | Out | In | Out | In | Out | In | Out |
---|
Alternaria | 15 | 30 | 62.7 | 58.8 | 38 | 65 | 82 | 82 | 53.8 | 61.5 | 64 | 53 | 38 | 3.8 | 35 | 29 |
Aspergillus spp. | 100 | 100 | 94.1 | 82.4 | 100 | 100 | 70.6 | 64.7 | 100 | 92.3 | 100 | 88.2 | 96.2 | 88.5 | 100 | 100 |
Cladosporium | 84.6 | 88.4 | 100 | 100 | 65 | 53.8 | 100 | 100 | 34.6 | 42 | 64 | 53 | 84 | 88 | 100 | 100 |
Fusarium | 19 | 15 | 47 | 53 | 30 | 53 | 93 | 76 | 30 | 38 | 88 | 88 | 11.5 | 0 | 58 | 64 |
Penicillium | 96 | 100 | 94 | 100 | 92 | 84 | 94 | 94 | 46 | 53 | 100 | 88 | 50 | 88 | 100 | 100 |
Yeasts | 15 | 15 | 70 | 47 | 84 | 69 | 82 | 100 | 46 | 50 | 64 | 64 | 1 | 2 | 47 | 41 |
Other | 100 | 100 | 100 | 100 | 100 | 100 | 100 | 100 | 100 | 100 | 100 | 100 | 100 | 100 | 100 | 100 |
The indoor to outdoor ratio is used to compare the distribution and assess the potential sources of fungi. In the present study, most of the I/O ratios were close to one, with the slightly higher values in the rural area (
Table 3) suggesting that not all indoor fungi originated from outdoors, which could be an indication of lesser indoor air quality. Hidden mold conditions, grains storage, dusty air and building materials may play a role in increased indoor fungal concentrations in the rural homes. The lowest I/O ratio that was found in the winter in the rural area may be attributed to less opening of windows that reduces outdoor infiltration of fungal organisms and decreases the presence of indoor dusty air from outdoor agricultural activities. On the other hand the lowest I/O ratio in urban area detected in autumn could be a result of increasing plant debris in the outdoor environment contributing to fungal concentrations outdoors.
In the present study, fungal concentrations were found to be higher than those reported in previous studies around the world. Indoor and outdoor concentrations, respectively, averaged 82 CFU/m
3 and 540 CFU/m
3 across the US [
26]; 89 CFU/m
3 and 68 CFU/m
3 in Cincinnati, OH, USA [
27]; and 812 CFU/m
3 and 1,042 CFU/m
3 in Latrobe Valley, Australia [
28]. Although results of several studies are similar to those of our study with indoor and outdoor concentrations, respectively, in 820 healthy (or reference homes) residential buildings ranged between 68–2,307 CFU/m
3 and 400–80,000 CFU/m
3 in the USA [
29] and 264–17,788 CFU/m
3 and 123–5,771 CFU/m
3 in Mexico [
30]. Moreover, in Egypt, fungal concentrations were found in the range of 10–10
2 CFU/m
3 in the indoor air of the Church of Saint Katherine Monastery in Sinai [
31], and 52–124 CFU/m
3 indoors and 25–222 CFU/m
3 outdoors at the coastal buildings in Domitta [
32].
There are no guidelines for airborne fungi, however a number of numeric guidelines have been proposed throughout the years [
29,
33,
34,
35,
36], but none of them are currently widely accepted by the scientific community [
7]. In comparison with the previously suggested guidelines, our findings indicated that the Egyptian
’s homes had much higher than acceptable levels of fungi. The indoor air quality of the Egyptian
's homes may be considered a poor since fungal concentrations exceeded 500 CFU/m
3 suggested by the World Health Organization [
35] and Singapore [
36] as well as 200 CFU/m
3 by the American Conference of Governmental Industrial Hygienists [
37]. In the present study, fungal concentrations in the size range of ≤8 µm (84.26%) was the predominant fraction. This was similar to the respirable fungal fraction concentrations that accounted for 70–80% of the total fungi in American and Taiwanese homes [
2,
38,
39], and 79–98% in Mexico [
30].
In most parts of the world the main core of fungal aerosols is likely to be similar, but the dominance of genera may differ from one area to another depending on geographical location, local sources, and climatic conditions [
40]. Qualitative determination of fungi may be more useful than determining concentrations, as many species may have health effects. The frequent detection of
Aspergillus spp.,
Penicillium, and
Cladosporium is attributed to their ready dissemination into the air. These findings in our study are similar to those observed in other geographical locations in Italy [
41], Egypt [
32,
42], and Florida, USA [
7].
Horner
et al. [
4] grouped fungi into three categories with different ecological relevance: (1) phyloplane fungi (
Cladosporium,
Curvularia and
Alternaria); (2) soil fungi (
Penicillium,
Paecilomyces and
Aspergillus), and (3), water indicator fungi (
Chaetomium,
Stachybotrys and
Ulocladium). In the present study water indicator fungi were found in low counts, and their presence associated with rain time or the presence of damped materials, however phyloplane and soil fungi were found in higher counts in the rural environment.
Cladosporium contains species that commonly grow indoors (
C. sphaerospermum) and outdoors (
C. cladosporioides and
C. herbarum) [
43]. Yeasts and
Cladosporium dominate healthy homes while
Absidia and
Alternaria are more likely in moldy homes, and
Penicillium and
Cladosporium in both healthy and moldy homes [
14].
Alternaria has an affinity for outdoor substrates, and when its I/O ratio exceeds one, this could indicate the presence of abnormal indoor conditions. The presence of
Aureobasidium and
Eurotium in rural homes is an indication of the presence of cellulotic materials and bad storage conditions, respectively. Moreover, the presence of some fungal species in indoor not outdoors mainly
Stachybotrys may indicate hidden mold conditions particularly in the rural homes.
Regarding season,
Cladosporium,
Penicillium and yeasts dominated in the winter, while
Aspergillus spp. in the summer. High concentrations of
Aspergillus spp. and
Alternaria in the autumn are associated with the decaying vegetable materials [
44].
Penicillium was found in the highest concentration in the months with low temperatures, as precipitation seemed to optimize their sporulation [
45]. Hargreaves
et al. [
46] isolated maximum concentrations of
Alternaria in the spring, as the suitability of humidity and temperature and vegetation debris [
25].
Cladosporium, Penicillium and Alternaria could increase the risk of asthma and allergic rhinitis and allergic alveolitis [
47].
Acremonium,
Alternaria,
Aspergillus,
Cladosporium,
Fusarium,
Paecilomyces,
Penicillium,
Stachybotrys and
Trichoderma are well known mycotoxin producers [
48].
Aspergillus flavus and
Aspergillus fumigatus can lead to aspergillosis [
49], and
Microsporium and
Trichophyton are agents of dermatophytoses [
50]. As the potential implications of the fungal contamination on health have not been studied in Egypt, it should to be reported that exposure to such concentrations and types is a risk factor for resident’s respiratory symptoms.
In the present study, the results represent the normal mycoflora in non-problem homes and describe the typical background concentrations in the indoor air environment. It should be mentioned that, the main limitations in the present study were: (1) short indoor sampling times that may not provide representative samples or accurately reflect exposures; (2) outdoor samples may not be representative since the apartment complexes restricted the airflow; and (3) geographical regions were large and could contain localized sources, and (4) explanations in discussion section regarding fungal concentration variations are speculation and not supported by local measurements. However, we believe that all buildings should be thoroughly inspected for visible signs of moisture. In addition good ventilation, household maintenance, minimizing dust generation and applying a proper and routine cleaning should be applied.