O A

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Advances in Environmental Biology, 5(11): 3645-3652, 2011
ISSN 1995-0756
This is a refereed journal and all articles are professionally screened and reviewed
ORIGINAL ARTICLE
The Determination of Airborne Fungal Flora of Two Different Hospitals in Istanbul
(Turkey)
1
Günay COLAKOGLU, 2Iskender KARALTI
1
Marmara University, Faculty of Science and Letters, Department of Biology, Ziverbey, 34722. Istanbul,
Turkey.
2
Yeditepe University, Faculty of Medicine, Medical Microbiology, 34755. Istanbul, Turkey.
Günay COLAKOGLU, Iskender KARALTI: The Determination of Airborne Fungal Flora of Two
Different Hospitals in Istanbul (Turkey).
ABSTRACT
The current study was carried out on monthly fungal flora of Marmara University Hospital and Goztepe
Education and Research Hospital in Istanbul between 2005 and 2006. The Petri-plate method based on gravity
was used for isolation. A total of 175 fungal colonies were isolated from Marmara University Hospital and the
maximum isolation was in May and the minimum isolation was in February. Species isolated from Marmara
University Hospital; are Cladosporium (42.9%), Alternaria (18.9%), Penicillium (12.6%), Aureobasidium
(11.4%), Aspergillus (6.9%), Mycelia Sterilia (4.6%), Scopulariopsis (1.7%), Rhizopus (0.6%) and Ulocladium
(0.6%). A total of 182 fungal colonies were isolated in Goztepe Education and Research Hospital and the
maximum isolation was in May and the minimum isolation was in January. Isolated species are; Cladosporium
(32.4%), Alternaria (24.2%), Penicillium (15.9%), Aureobasidium (9.3%), Aspergillus (7.1%), Scopulariopsis
(3.8%), Ulocladium (3.3%), Mycelia Sterilia (2.7%), Rhizopus (0.5%) and Paecilomyces (0.5%). A number of
fungal species with pathogenic potential were encountered among the species isolated in this study. The results
obtained from the species distribution showed that there were no differences between the two hospitals.
Key words: Mould, Airborne Fungi, Mould Flora, Hospital Air, Indoor Air.
Introduction
There are plenty of fungi in air [18]. Since
spores, which are reproduction structures of fungus,
can easily be spread in air. They amply exists both
indoor and outdoor environments [5,25].
Occurrence probability of moulds in clinical
environments is very high Shelton et al., [39].
Moulds can cause many illnesses such as respiratory
tract sickness, allergic reactions, sinusitis and
hospital infections time to time in people [46,27]. At
the same time, higher density of moulds in clinical
environment
is
risky
in
terms
of
immunocompromised patients (HIV carriers,
oncology patients) and old patients. And especially,
Aspergillus caused by certain types of Aspergillus
species, is seen in chemotherapy patients rather
frequently [34,42]. Therefore mould flora
determination of hospitals air is important.
Most important ones among allergen fungus
spores, which are effective on respiratory tract
allergens are Cladosporium, Alternaria, Aspergillus
and Fusarium [9,38,17]. Determination of these
moulds period and densities in atmosphere is very
important for sensitive individuals  [26].
Moulds can reproduce under many different
environmental niches such as soil, plant and water. It
is known the relationships between spore production
and
environmental
conditions,
such
as
meteorological factors [29]. Their concentrations are
affected by wind, humidity, temperature, rain,
altitude and vegetation. Fungus density becomes
dense in humid environments, especially in cloudy
and humid atmospheres fungus densities become
high [13].
Material and Method
Material (Collection of Samples):
Samples were collected in between February
2005 and January 2006 for one year of duration from
parts of Marmara University Hospital and Goztepe
Education and Research Hospital, denoted in Table1.
Table 1: Installments where Samples has been collected.
1. Microbiology Laboratory
2. Toilets
3. Waiting rooms
4. Hospital gardens
5. Libraries
Corresponding Author
Günay COLAKOGLU, Marmara University, Faculty of
Biology, Ziverbey, 34722. Istanbul, Turkey.
E-mail: [email protected]
Science and Letters, Department of
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Adv. Environ. Biol., 5(11): 3645-3652, 2011
The samples were collected monthly from the
denoted parts of given hospitals for one year. Petri
Plaque method based on gravity (settle plates
method) was used for sample collection. Samples
were collected by opening Petri dishes for 15-30
minutes at specified areas at 75-85 cm elevation from
the ground. Samples were collected in the morning
between 07:30-09:30. Windows were closed during
the indoor collection of material. Consequently
outdoor contaminations were prevented. This process
were applied in 5 different places of specified
hospitals during the year. Peptone Dextrose Agar
was used as the culture medium while collecting the
samples. 30 mg/l streptomycin had been added to the
culture to prevent bacteria reproduction [14]. RoseBengal stain was added to the culture in order to
prevent faster reproduction of moulds [37,38].
Method:
Plaques containing Peptone Dextrose Agar
which was used for isolation, was put into 7 days of
incubation in laboratories at room temperature (2226 ºC). Later, every reproduced fungus colony had
been put into Potato Dextrose Agar (PDA), Malt
Extract Agar (MEA) and Czapek’s Agar (CZA) by
utilizing passage to the culture mediums. These
plaques were also put into incubation for 7 days at
room temperature (22-26 ºC). After the incubation
pure cultures of microfunguses were obtained.
Meanwhile, surface and inverse appearances of
colonies and colony diameters were noted and
exudation and pigmentation statuses were examined
[14]. Lactophenol solution stained by picric acid and
lactophenol solution stained by cotton blue was used
for investigation of microscopic structures of moulds
[10]. Preparates, made of pure cultures was examined
at microscope. Various structures of microfunguses
measured for 50 times and averaged.
Identification of funguses were tried to be
performed by making use of domestic and foreign
resources. In distinguishing the genus, the resource
named of “Illustrated Genera of Imperfect Fungi”
was used (Barnett, 1987). It was used for
identification of Rhizopus species; ”Mucorales”
Zycha, [47] for Aspergillus species;‘’ The Genus
Aspergillus’’ [35] and ‘’List of accepted species and
their synonyms in the family Trichocomonaceae’’
Pitt, [33]
for Penicillium, Gliocladium,
Paecilomyces species; A Manual of the Penicillia’’
[36], for Alternaria, Cladosporium, Ulocladium,
Aureobasidium,
Scopulariopsis
species;
‘’Dematiaceous Hypomycetes’’ Ellis, [20] and
Simmons [40], for Fusarium species; ‘’ The Genus
Fusarium’’ Booth, [11] for
Mycelia sterilia;
‘’Ainsworth & Bisby’s Dictionary of the
Fungi’’Ainsworth, [2] and ‘’Tohumsuz Bitkiler
Sistematiği’’
(Bacteriophyta,
Cyanophyta,
Phycophyta, Mycophyta, Lichenes) [19].
Determination of relation between temperature
and fungus density, in the study; temperature and
humidity values of sampling areas has been
measured via thermometer and hygrometer. These
values are given in Table 2-3.
Results:
175 mould colonies were isolated in Marmara
University Hospital and allergenic ones were
speciated (Table 4). Maximal mould isolation was
occurred in May, and minimal in February. Mostly
isolated species was Cladosporium (42.9%). This
one were followed by Alternaria (18.9%),
Penicillium (12.6%), Aureobasidium (11.4%),
Aspergillus (6.9%), Mycelia Sterilia (4.6%),
Scopulariopsis (1.7%), Rhizopus (0.6%) and
Ulocladium (0.6%).
Maximally isolated species in this hospital
during the study was Cladosporium cladosporioides
(36.6%).
Table 2: Measured humidity and temperature values of sampling areas of Marmara University Hospital sample research (February
January 2006).
Marmara University Hospital
1
2
3
4
5
Months
T
H
T
H
T
H
T
H
T
February
19
49
15
51
15
51
9
50
15
March
20
55
16
54
15
53
10
55
15
April
19
41
17
43
17
42
12
40
16
May
20
80
21
81
23
80
21
79
21
June
21
71
21
72
21
71
21
70
22
July
24
67
27
70
27
70
28
69
27
August
24
61
26
64
27
65
29
71
27
September
23
75
24
73
25
72
23
77
26
October
22
82
19
83
18
83
15
82
20
November
20
90
17
91
17
90
14
92
19
December
18
61
19
61
17
62
8
60
18
January
18
41
17
40
16
42
5
40
17
T: Temperature (C) , H: Humudity (%)
1. Microbiology Laboratory, 2. Toilets, 3. Waiting saloons, 4. Hospital gardens, 5. Libraries
2005-
H
51
54
41
80
71
70
64
77
80
93
63
41
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Adv. Environ. Biol., 5(11): 3645-3652, 2011
Table 3: Measured humidity and temperature values of sampling areas of Göztepe Education and Research Hospital sample research
(February 2005- January 2006).
Göztepe Education and Research Hospital
1
2
3
4
5
Months
T
H
T
H
T
H
T
H
T
H
February
18
44
15
50
16
52
8
51
15
52
March
20
55
15
54
14
53
10
56
14
53
April
19
41
16
44
16
42
12
41
15
42
May
20
80
20
82
23
79
21
80
21
80
June
20
70
22
73
22
70
21
70
22
72
July
26
70,5
28
71
28,5
71
27
75
26
71
August
25
65
27
66
26
66
26
65
27
67
September
25
71
26
71
25
72
23
73
26
73
October
23
83
16
85
16
85
14
84
18
88
November
20
77
17
79
17
80
16
78
22
83
December
18
62
19
62
17
62
8
60
17
62
January
18
41
18
41
15
43
5
41
18
43
T: Temperature (C) , H: Humudity (%)
1. Microbiology Laboratory, 2. Toilets, 3. Waiting saloons, 4. Hospital gardens, 5. Libraries
Table 4: Colony Numbers and Percentages of Total Microfungus Species in Marmara University Hospital during February 2005-January
2006 period.
Number of
Genera and species name
colony
%
The month which was isolated
Installment where was isolated
Alternaria
33
18.9
M,A,Ma,Ju,Jl,Au,S
3.4
Alternaria alternata*
31
17.7
M,A,Ma,Ju,Jl,Au,S
3,4,5
Alternaria tenuissima
2
1.1
Jl,S
4
Aspergillus
12
6.9
F,M,A,Ma,Ju,Jl,Au
1,2,3,4,5
Aspergillus candidus
1
0.6
A
4
Aspergillus cervinus
1
0.6
M
4
Aspergillus flavus*
1
0.6
F
1.4
Aspergillus nidulans
3
1.7
M,Au
4.5
Aspergillus niger*
5
2.9
A,Ma,Ju,Jl
2,3,4,
Aspergillus reptans*
1
0.6
F
4
Aureobasidium
20
11.4
M,A,Ma,Ju
2,3,4
Aureobasidium pullulans*
20
11.4
M,A,Ma,Ju
2,3,4
Cladosporium
75
42.9
J,F,A,Ma,Ju,Jl,Au,S,O,N,D
1,2,3,4,5
Cladosporium cladosporioides*
64
36.6
J,F, A,Ma,Ju,Jl,Au,S,O,N,D
1,2,3,4,5
Cladosporium herbarum*
8
4.6
J,F,O,N,D
3.4
Cladosporium oxysporum
3
1.7
Ma
4
Mycelia sterilia
8
4.6
Jl,N
4.5
Penicillium
22
12.6
J,F,M,Au,S,O,N,D
1,2,3,4,5
Penicillium brevicompactum
8
4.6
J,S,N,D
1,3,4
Penicillium citrinum
5
2.9
J,F,M,Au
1,4,5
Penicillium commune
3
1.7
J,O,N,D
4,5
Penicillium digitatum
2
1.1
F
4
Penicillium glabrum*
3
1.7
J,D
2,4
Penicillium notatum
1
0.6
F
4
Rhizopus
1
0.6
O
4
Rhizopus nigricans*
1
0.6
O
4
Scopulariopsis
3
1.7
M,D
4.5
Scopulariopsis brevicaulis
1
0.6
M
4
Scopulariopsis brumptii
2
1.1
D
4.5
Ulocladium
1
0.6
Jl
4
Ulocladium botrytis
1
0.6
Jl
4
Toplam
175
100
J : January, F :February, M: March, A:April, Ma: May, Ju: June, Jl:July, Au: August, S: September, O: October,
N: Nowember, D: December
1. Microbiology Laboratory, 2. Toilets, 3. Waiting rooms, 4. Hospital gardens, 5. Libraries
* Microfungus types specified as allergen [15].
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Adv. Environ. Biol., 5(11): 3645-3652, 2011
80
75
70
60
Cl ado spo rium
50
Al ternaria
40
Penicillium
33
30
Aureobasidium
22
20
20
As perg illus
12
10
0
Fig. 1: Monthly Distribution of Colony Numbers of Total Microfungus Species Isolated in Marmara University
Hospital (February 2005-January 2006).
39
24
9
21
13
11
11
13
17
8
5
JU
LY
A
U
G
S
U
E
S
P
T
TE
M
B
E
R
O
C
TO
B
E
N
R
O
V
E
M
B
D
E
E
R
C
E
M
B
E
R
JA
N
U
A
R
Y
JU
N
E
M
A
Y
4
A
P
R
İL
45
40
35
30
25
20
15
10
5
0
FE
B
R
U
A
R
Y
M
A
R
C
H
Number of colony
Number of colony
Months
Number of colony
Fig. 2: Colony Counts of Total Microfungus Species in Marmara University Hospital (February 2005-January
2006).
182 mould colonies were isolated in Göztepe Education and Research Hospital and allergen ones was
specified (Table 5). Maximal mould isolation was occurred in May, and minimal in January. Isolated species
are; Cladosporium (32.4%), Alternaria (24.2%), Penicillium (15.9%), Aureobasidium (9.3%), Aspergillus
(7.1%), Scopulariopsis (3.8%), Ulocladium (3.3%), Mycelia Sterilia (2.7%), Rhizopus (0.5%) and Paecilomyces
(0.5%). Maximally isolated species in this hospital during our study was Cladosporium cladosporioides
(23.6%).
Fig. 3: Monthly Distribution of Colony Numbers of Total Microfungus Species Isolated in Goztepe Education
and Research Hospital (February 2005-January 2006).
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Adv. Environ. Biol., 5(11): 3645-3652, 2011
Table 5: Colony Numbers and Percentages of Total Microfungus Species in Göztepe Education and Research Hospital during February
2005-January 2006 period.
Genera and species name
Number of colony %
The month which was isolated Installment where was isolated
Alternaria
44
24.2
F,M,A,Ma,Ju,Jl,Au,S
1,2,3,4,5
Alternaria alternata*
36
19.8
F,M,A,Ma,Ju,Jl,Au,S
1,2,3,4,5
Alternaria tenuissima
8
4.4
Ju,Jl, Au,S
3,4
Aspergillus
13
7.1
J,F,M,A,Ma,Ju,S,N,D
1,2,3,4,5
Aspergillus candidus
2
1.1
J,F,N,D
1,2,4
Aspergillus flavipes
1
0.5
J,F
4,5
Aspergillus fumigatus*
1
0.5
J,F
1,3
Aspergillus nidulans
3
1.6
F,M,A
2,3,4
Aspergillus niger*
3
1.6
J,F,M,Ma
4,5
Aspergillus ochraceus
1
0.5
S
4
Aspergillus restrictus
1
0.5
F,D
4
Aspergillus ustus
1
0.5
Ju
4
Aureobasidium
17
9.3
M,A,Ma,Ju,Jl,Au
1,2,3,4
Aureobasidium pullulans*
17
9.3
M,A,Ma,Ju,Jl,Au
1,2,3,4
Cladosporium
59
32.4
J,F,M,A,Ma,Ju,Jl,Au,S,O,N,D 1,2,3,4,5
Cladosporium cladosporioides*
43
23.6
F,M,A,MA,Ju,Jl,Au,S,O,N,D
1,2,3,4,5
Cladosporium herbarum*
11
6.0
J,A,Ma,Jl,Au,S
3,4,5
Cladosporium sphaerospermum*
5
2.7
Ma,Ju
4
Mycelia sterilia
5
2.7
Ma,Jl,O
4
Penicillium
29
15.9
J,F,M,A,Ma,Ju,Au,S,O,N,D
1,2,3,4,5
Penicillium brevicompactum
4
2.2
J,F,N,D
1,3,4
Penicillium chrysogenum*
1
0.5
F,Ma
4,5
Penicillium citrinum
1
0.5
J,S
4
Penicillium commune
3
1.6
F,O,N,D
2,3,4
Penicillium glabrum*
20
11.0
J,F,M,Ma,Ju,Au,N,D
1,2,3,4,5
Paecilomyces
1
0.5
S
4
Paecilomyces sp.
1
0.5
S
4
Rhizopus
1
0.5
J,A,N
3,4
Rhizopus nigricans*
1
0.5
J,A,N
3,4
Scopulariopsis
7
3.8
M,A,Jl,Au,S
2,3,4,5
Scopulariopsis brevicaulis
3
1.6
M,A,Au
2,3,4
Scopulariopsis brumptii
4
2.2
Jl,S
4,5
Ulocladium
6
3.3
Ju,Jl,Au
3,4
Ulocladium botrytis
6
3.3
Ju,Jl,Au
3,4
Toplam
182
100
J: January, F: February, M: March, A: April, Ma: May, Ju: June, Jl: July, Au: August, S: September, O: October, N: Nowember, D:
December
1. Microbiology Laboratory, 2. Toilets, 3. Waiting rooms, 4. Hospital gardens, 5. Libraries
* Microfungus types specified as allergen [15].
60
50
59
44
Cladosporium
40
30
Alternaria
29
20
Penicillium
Aureobasidium
17
13
Aspergillus
10
0
Fig. 4. Colony Counts of Total Microfungus Species in Goztepe Education and Research Hospital (February
2005-January 2006).
When the annual mould flora of the two
hospitals has been compared, it is observed that
monthly distributions are close to each other.
Maximally isolated species in both hospitals were
Cladosporium, Alternaria, Penicillium, Aspergillus
and Aureobasidium. The most isolated species in
both hospitals is found as Cladosporium
cladosporioides (Table 4, 5).
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Adv. Environ. Biol., 5(11): 3645-3652, 2011
Discussion:
Moulds can live in very different environmental
conditions [6]. They can be found in hospital like
crowded environments, since they can easily spread
in air via their reproduction structure spores. Moulds
can cause sicknesses such as respiratory tract
infections, aspergilloz, asthma, allergic reactions and
sinusitis in humans [21]. Therefore excess amounts
of moulds in air entertain risk for patients [26,8].
While number of suppressed immune system patients
is increasing because of cancer, chemotherapy and
AIDS, number of fungus infections is also increasing
[46]. Concerns on moulds had been increased
recently, since diagnostic of mould infections is hard,
have long term therapy period; and studies on this
subject are also increasing with time [26,21].
In many studies up to now, it was specified that
mould density in air is in relation with humidity and
temperature of the air, and mould density increased
with increasing temperature and humidity [44,1].
And mould density increases in Istanbul city in
spring, summer and autumn seasons [15]. When the
temperature and humidity values (Table 2, 3) and
was isolated colony numbers (Graphics 1, 3),
identified in our study, and was examined; it was
found that temperature and humidity directly affect
fungus concentration. When the monthly distribution
(Graphics 1, 3) of isolated funguses examined, it was
seen that maximal mould isolation occurs in May in
both of the hospitals. It was found that, in May,
average measured humidity ratio is 80% and
temperature is 21.2 °C in Marmara University
Hospital; and average was measured humidity ratio is
80% and temperature was 21 °C in Göztepe
Education and Research Hospital. Minimal isolation
occurred in winter in our study.
Maximally isolated moulds in studies performed
in Turkey; were given as Cladosporium, Aspergillus,
Penicillium,
Alternaria
and
Aureobasidium
[25,5,37]. In our study, in Marmara University
Hospital mostly Cladosporium (42.9 %) were
isolated. This was followed by Penicillium (% 23.4),
Aureobasidium
(%12.0),
Alternaria
(%7.4),
Aspergillus (%7), Mycelia sterilia (%4.6),
Scopulariopsis (%1.7), Rhizopus (%0.6) and
Ulocladium (% 0.6). (Table 4). In Goztepe Education
and Research Hospital, mostly Cladosporium (%
32.4) was isolated. It was observed that this is
followed by Alternaria (% 24.2), Penicillium (%
15.9), Aureobasidium (% 9.3), Aspergillus (% 7.1),
Scopulariopsis (% 3.8), Ulocladium (% 3.3), Mycelia
sterilia (% 2.7), Rhizopus (% 0.5) and Paecilomyces
(% 0.5). (Table 5). In both hospitals, mostly
Cladosporium was isolated (Graphics 2, 4).
And in foreign studies were reported that mostly
isolated funguses were Cladosporium, Aspergillus,
Penicillium,
Alternaria,
Aureobasidium
[43,32,3,30,28,31].
Aspergillus and Penicillium were observed at
higher levels in autumn and winter season; and at
lower levels in summer season. Alternaria and
Cladosporium were observed at higher levels in
summer season; and at lower levels in winter season.
This situation was identified both by different
domestic and foreign researchers [99]. In the study,
which was performed in Izmir, the types belong to
Aspergillus species was continuously isolated during
the study [12]. In our study was found same results.
In our study maximally isolated species in
Marmara University Hospital was Cladosporium
cladosporioides (36.6%), and this one was followed
by Penicillium commune (%12.6), Aureobasidium
pullulans (%12.0), Alternaria alternata (% 6.3),
Cladosporium herbarum (% 4.6), Penicillium
brevicompactum (%4.6), Aspergillus niger (%2.9),
Penicillium citrinum (%2.9). Isolated species in
Goztepe Education and Research Hospital were
respectively; Cladosporium cladosporioides (%
23.6), Alternaria alternata (%19.8), Penicillium
glabrum (%11.0), Aureobasidium pullulans (%9.3),
Cladosporium herbarum (%6.0), and Alternaria
tenuissima (%4.4). When the fungus colony numbers
isolated in both hospitals were compared, it was seen
that they were lose to each other (175 colonies in
Marmara University Hospital and 182 colonies in
Göztepe Education and Research Hospital were
isolated). And when the species distribution was
concerned, there were no different results.
Fungal flora of crowded places where people
applied for their health such as hospitals should be
determined and controlled routinely.
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