Indoor and Built Environment

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The Relationship between Moulds Isolated from Indoor Air and Features of the House Environment A. Ozkutuk, E. Ceylan, G. Ergor, M. Yucesoy, O. Itil, S. Caymaz and A. Cimrin Indoor and Built Environment 2008; 17; 269 DOI: 10.1177/1420326X08091958 The online version of this article can be found at: http://ibe.sagepub.com/cgi/content/abstract/17/3/269

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Original Paper

Indoor and Built Environment

Indoor Built Environ 2008;17;3:269–273

Accepted: January 22, 2008

The Relationship between Moulds Isolated from Indoor Air and Features of the House Environment A. Ozkutuka E. Ceylanb G. Ergorc S. Caymaza A. Cimrind

M. Yucesoya O. Itild

a Department of Microbiology and Clinical Microbiology, Dokuz Eylul University, Izmir b Department of Pulmonary Medicine, Adnan Menderes University, Aydin c Department of Public Health, Dokuz Eylul University, Izmir d Department of Pulmonary Medicine, Dokuz Eylul University, Izmir

Key Words Moulds E Indoor air E House characteristics.

Abstract In an attempt to determine the relationship between the features of houses and moulds growing indoors, 242 houses were examined in Izmir, a city on the west coast of Turkey with a mild climate. During house visits a questionnaire was given and air was sampled using an ‘air IDEAL’ air sampler for quantitative fungal culture. The moulds most commonly isolated were Aspergillus, Penicillium, and Mucor spp. Aspergillus growth in houses older than 20 years was more common than other species when the features of houses and isolated fungi were compared. Mucor grew significantly more in houses where the air was humid, the temperature was cooler and there were pot plants. Penicillium grew more frequently in houses where visible mould was present and birds were bred. However, no relationship could be demonstrated between the method of heating, the number of household members, exposure to sun, type

SAGE Publications 2008 Los Angeles, London, New Delhi and Singapore DOI: 10.1177/1420326X08091958 Accessible online at http://ibe.sagepub.com

of building and flooring with a specific mould. As a conclusion, many household factors suggested as risk factors for mould growth have been examined and only a few relationships could be established between certain features of houses and moulds. However, mould growth is much affected by many conditions and the environment in a house is one of many factors that may facilitate growth.

Introduction Moulds are widely found throughout nature. However, their presence in a house can cause serious respiratory side effects in the inhabitants. There are numerous studies reporting relationships between presence of household moulds and coughing, dyspnea, asthma, and development of many allergic diseases [1–3]. Type and amount of household moulds vary according to the aeration, temperature, and humidity of the environment, presence of pets and/or plants at home. Studies have

A. Ozkutuk Department of Microbiology and Clinical Microbiology, Dokuz Eylul University School of Medicine, 35340, Inciralti-Izmir, Turkey. Tel. (9.0232) 4124510, Fax þ 90.232.4124501, E-Mail [email protected], [email protected] Downloaded from http://ibe.sagepub.com at Dokuz Eylul Universitesi on September 15, 2008

been conducted in every part of the world investigating the environment of houses and presence of mould [4–10]. Determining relevant features of houses in detail by questionnaires and house visits, confirming the presence of moulds quantitatively and establishing the type of the mould can yield important information for assessing any relationship between house features and moulds. The aim of the present study was to determine the moulds present in indoor air in Izmir, a city with a moderate climate and to establish any relationships between these fungi and the features of the houses.

Materials and Methods

Statistical Analyses Results were analyzed using SPSS v10.0 statistical package. Associations between home characteristics and moulds were analyzed by chi-square tests. Continuous variables were analyzed using Student’s t-test. Significance was accepted for p-values lower than 0.05.

Results

Sample Selection Present study looked at the same 242 houses that were used in a previous study [11]. These houses belonged to 127 asthma patients followed-up by the Out-patient Clinic for Pulmonary Diseases of Dokuz Eylul Training and Research Hospital and their 115 healthy neighbors. Obtaining Air Samples Appointments were made on the phone before visiting the selected houses and the owners were asked not to aerate their houses for the day of the visit. Air samples were taken between 15 January and 30 March during house visits made between 09:00 and 13:00 h. A physician took air samples, administered the questionnaire and observed the features of the house. An ‘‘air IDEAL’’ (bioMe´rieux, Marcy l’Etoile, France) air suction device was used to obtain samples. One hundred and fifty liters of air was sucked through the machine from the living rooms of each house and sprayed onto Malt Extract agar media (MEA; Oxoid Ltd., Basingstoke, Hampshire, UK). Fungal Examination Media sprayed with air were incubated for 10 days at 258C and were observed from day 4 and onwards. Colonies that grew were identified based on macroscopic and microscopic characteristics. Fungi isolated from air samples obtained from houses were expressed as cfu m3. Questionnaire and Household Observation During house visits, temperature, and humidity were measured by thermometer and TFA hygrometer (TFADostmann Gmbh, Germany), respectively. Houses were examined for the presence of visible mould. Information on the features of the house including the type and age of

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the building, type of flooring, method of heating, whether or not the house gets direct sunlight, presence of pets and plants and the number of people in the household was acquired using the questionnaire.

Indoor Built Environ 2008;17:269–273

The mean amount of moulds found in the indoor air of the houses was 35.45 10.4 cfu m3. Significant relations between the type of mould and total mould density were not identified. However, the median indoor fungal concentration was significantly higher in houses who grew Mucor and Alternaria (for Mucor 41.7 7.3/34.3 10.5; p ¼ 0.000 and for Alternaria 40.8 10.8/34.6 10.1cfu/m3; p ¼ 0.004). The order of the frequency of fungi isolated was Aspergillus (41%), Penicillium (24%), Mucor (9%), Alternaria (7%), Chrysosporium (5%), Fusarium (3%), Acremonium (3%), and others (8%). Other fungi included Cladosporium, Ulocladium, Stemphylium, Aureobasidium, Paecilomyces, Scedosporium, Scopuloriopsis, Monilia, Epicoccus, Nigrospora, Pseudoallescheria boydii, Rhizopus, and Trichotechium. Fungi isolated from sampled air are presented in Figure 1. There was some relationship determined between visible mould in any part of the house and the home characteristics. House related factors and their relationship to current visible mould are shown in Table 1. When the features of the houses were assessed, fungal growth was significantly higher when the age of the building was advanced ( p ¼ 0.04). Growth of Aspergillus was higher than other species in buildings older than 20 years. However, this relationship was not statistically significant ( p: 0.008). There was also no relation in favor of moulds regardless of the type of building, whether it was a detached house or an apartment. When the growth pattern was compared with respect to the floor, Chrysosporium, and Alternaria grew significantly higher than other species on ground floors where denser growth was also observed ( p ¼ 0.02). Comparisons with regard to the floor covering revealed significantly higher fungal growth on stone and marble

Ozkutuk et al.


8% 3% 3% 5% 41% 7%

9%

Aspergillus Pencillium Mucor Alternaria Chrysosporium Fusarium Acremonium Other fungi

24%

Fig. 1. Fungi isolated from air samples.

Table 1. House related factors and their relationship to current visible mould Mould reported in any room of the house

No mould reported in the house

19.8* 62% 20.0* 48.7* 3.4

16.9 77%* 22,0 43.8 3.0

11% 63% 27% 5.4 10% 21% 50% 17% 30%* 71% 14%

23%* 65% 12% 5.2 28%* 21% 55% 14% 7% 93%* 15%

House age (years) Sunlight exposure in winter (n) Room temperature (8C) Relative humidity (%) Number of residents in the house (n) Income level High Middle Low Total fungi (cfu/m3) Central heating (%) Existence of air conditioning (n) House plants (%) Presence of pet (n) House (n) Apartment (n) Insulation in the house (n)

Table 2. The sources of humidity in the houses

Poor insulation (floor, walls, roof) Insufficient ventilation Drying clothes in the room Repair of water pipes All reasons included Total

n

(%)

76 65 60 35 5 241

32.6 27.0 24.9 15.7 0.8 100.0

floors compared to wooden floors ( p ¼ 0.01). On the other hand, significant relations between mould types and the type of floor covering were not observed. Indoor activities such as taking shower and cooking which increase dampness were determined as an important source of dampness existing in all houses. While the most important indoor sources of dampness were only activities like taking shower and cooking in 165 cases (68.2%), another additional source was drying laundry

for 76 cases (31.4%). The sources of dampness are shown in Table 2. Significant relations between the temperature and humidity of the houses and total mould density were not identified. However, among the moulds grew, Mucor grew significantly higher in humid and cooler (less than 218C) houses. The temperatures and humidities were significantly higher in these houses than in the others (not growing Mucor), respectively [19.8 3.18C; 21.4 3.58C ( p ¼ 0.006) and 49.2 10.7%; 45.3 11.2% ( p ¼ 0.04)]. One other mould that was related to the temperature was Chrysosporium. This mould tended to grow to a greater extent in houses where the temperature was higher than 228C. The temperatures of these houses were significantly higher than the others (23.6 4.28C/20.9 3.38C; p ¼ 0.001). However, the level of humidity was not statistically significantly different in these houses (45.0%; 46.0%; p ¼ 0.69). Compared to central heating, heavier mould growth was noted when local methods of heating were used. However, this growth was not statistically significant ( p ¼ 0.07).

Indoor Moulds and House Conditions


*p50.05.


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Table 3. House characteristics and their relationship with the type of fungi House conditions

Species of fungi

House age (n; year) Direct exposure to sunlight(%) Room temperature (mean 8C) Relative humidity (mean%) Pot plants (%) Presence of a pet (%) Current visible mold (%) Residents in the house (n) Floor covering Wooden floor Stone/marble floor Other Local heating (%)

Aspergillus

Penicillium

Mucor

Alternaria

18.9 68% 21.1 46.5 52% 13% 44% 3.2

17.5 65% 21.7 45.2 48% 18%* 50%* 3.2

18.5 64% 19.8* 49.2* 69%* 18% 49% 3.3

19.6 64% 21.5 45.5 46% 12% 39% 3.3

46% 34% 20% 20%

50% 36% 14% 23%

49% 31% 21% 15%

41% 41% 18% 18%

*p50.05.

Method of heating and exposure to sunlight did not produce any advantage in favor of a type of mould. There was no relation between the number of people in the household and mould growth. The effect of the presence of a pet in the house was less (15.3%) than for a pot flower (52.5%). When the relations between the types of mould and presence of a pet or pot flower at home were explored, we found that Mucor growth was significantly higher at houses with pot flowers present ( p ¼ 0.02). On the other hand, having pets at home was not significantly related to the types of moulds. However, Penicillium growth was significantly higher in the houses where residents had birds as pets (63.2%; p ¼ 0.05). Moreover, growth of Penicillium was significantly higher than other moulds when visible mould was observed ( p ¼ 0.04). The house characteristics and their relationship to the moulds are shown in Table 3.

Discussion Many studies have investigated the relation between the features of houses and fungal growth [5,6,12,13]. However, there are variations in the methods for sampling. For example, using the open Petri dish (OPD) method or air suction devices, both of which quantitative methods can be used for direct determination of fungal growth. Some of these studies rely on reports of fungal growth and have been conducted over the phone and/or using questionnaires. Here, fungal growth is detected indirectly while in

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some other studies it is planned and conducted prospectively [5,6,12,13]. In the present study, features of the houses were determined by a questionnaire and observation whereas fungal growth was determined quantitatively by obtaining air samples with an ‘air IDEAL’ air sampler. Verhoeff et al. [12] argued that, compared to OPD method, quantitative measurements performed using air sampling device yield more standard results to establish the presence of viable moulds. Gangneux et al. [14] were shown air sampler devices reliable for indoor sampling and no significant differences in fungal counts between various air sampler devices. In a pilot study, we found that more colonies grew with the quantitative method we used than the OPD method (unpublished data). In our study a significant relationship was not observed between amount of mould and current visible mould in any place of the house. We thought that quantitative analyses were more useful than the observation of moulds for comparing mould relationships with house characteristics. In the present study, the mean number of moulds isolated at houses was 35.45 10.4 cfu/m3. Most commonly isolated moulds were Aspergillus and Penicillium, followed by Mucor and Alternaria. Aspergillus and Alternaria have been reported to be the most important indoors and outdoors moulds, respectively [15]. Penicillium colonizes heating and air-conditioning systems and can cause asthma especially in children [16]. The Cladosporium sp. which are generally expected as the predominant fungi in outdoor air, were detected in much

Ozkutuk et al.


smaller numbers in the indoor air in the presented study. The climatic and regional factors, life style may have affected the survival and distribution of this genus in the houses. In our previous studies, we compared the houses of asthmatic patients with healthy controls and found no significant difference with respect to the density or the type of moulds [11]. Generally, indirect methods are used to determine the presence of humidity at homes (presence of water leak, visible mould, etc). In the present study, humidity measurements were carried out quantitatively using a TFA hygrometer. This has altered some results. For instance, when visible mould was taken as an indicator of humidity, a significant cohabitation with Penicillium was observed while, on the other hand, quantitative analyses revealed a relation between the degree of humidity and Mucor only. Here, a relation between general humidity and presence of visible mould could not be demonstrated. Literature on the relation between the features of houses and types of mould is scarce. Studies have mostly

concentrated on the features of houses and mould density [6–9]. Mucor, Penicillium, and Aspergillus growths were related to the presence of indoor pot plants, high humidity, and cooler room temperature; presence of visible mould and having birds as pets and age of building 420 years, respectively. Method of heating, the number in the household, direct exposure to sunlight, type of building and floor covering were not significantly related to any of the moulds. The level of fungal spores in the air varies according to the season [7,13]. Conducting the study in winter-spring decreased the total mould density indoors. The age of the building and stone-marble floor coverings significantly increased the total mould density. In conclusion, even though relationships have been found between certain features of houses and moulds, there are still a lot of unknowns. The data in this paper was obtained from a coastal town with a mild climate. Our results may vary depending on location, climate, and environment. Moreover, the rate of indoor growth of moulds is influenced by many outdoor factors as well.

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