Indoor fungi levels in homes of children with and without allergy history

Int. J. Hyg. Environ. Health 207 (2004); 369 ± 378http: //www.elsevier.de/intjhyg

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Snezana Jovanovica, Andrea Felder-Kennelb, Thomas Gabrioa, Bijan Kourose, Bernhardt Linka, Valentina Maisnerf,Isolde Piechotowskia, Karl-Heinz Schickc, Monika Schrimpfd, Ursula Weidnera, Iris Zˆllnera, Michael Schwenka

a State Health Agency (Landesgesundheitsamt), Stuttgart, Germanyb Health Department (Gesundheitsamt), Mannheim, Germanyc Health Department (Gesundheitsamt), Stuttgart, Germanyd Health Department (Gesundheitsamt), Offenburg, Germanye Social Ministry (Sozialministerium Baden-W¸rttemberg), Stuttgart, Germanyf Health Department (Gesundheitsamt), Ravensburg, Germany

Received August 6, 2003 ¥Revision received May 8, 2004 ¥Accepted May 20, 2004

��A study was performed at the four sentinel health departments of Baden-W¸rttembergbetween November 1999 and March 2000 to investigate the indoor levels of fungi at thehomes of school children (mean age 10 y) and to describe possible associations with allergystatuses. Three hundred and ninety-seven households of school children with (n�199) andwithout (n� 198) allergic history were included in the study. The median of colony formingunits (CFU/m3) of fungi, measured in the children's bedrooms' in indoor air, was 105 (range5 to 15000), in outdoor air 110 (range 10 to 1500). The median of viable mould spores(CFU/g dust) in floor dust was 28500 (range 1500 to 1235000), in mattresses 16250 (range 0to 2500000). Neither climatological conditions, nor differences between urban and ruralregions showed a systematic influence on fungi counts. There was no difference inconcentrations and distribution of fungi species levels between children with and withoutallergic history. The sensitization rate against molds (IgE) was higher for children withallergic condition (9.2%) than in control children (4.4%), but there was no association withthe fungi counts in the rooms. In conclusion, the study defined the mould levels in children'srooms, but did not find an association with allergic history of the children or theirsensitization rate.

Key words: Moulds ± children ± sensitization ± allergy screening - sentinel healthdepartments

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Indoormold contamination and its possible effect onhuman health especially in children are currentlymajor topics in environmental hygiene. In fact, fungi

are considered as a relevant risk factor for buildings(Santilli and Rockwell 2003) and their inhabitants.Though, associations between indoor dampness andallergic asthma, rhinitis, atopic dermatitis andrespiratory symptoms have been described in var-

1438-4639/04/207/04-369 $ 30.00/0

Corresponding author: Dr. Snezana Jovanovic, State Health Agency (Landesgesundheitsamt), Wiederholdstrasse 15,70174 Stuttgart, Germany. Phone: �49 711 1849310, Fax:� 49 711 1849242, E-mail: [email protected]

ious studies relying on self-reports or observations ofdampness (Brunekreef 1992; Bornehag et al. 2001),and there is considerable debate, whether fungi arethe actual cause (Chapman et al. 2003; Douwes andPearce 2003). Various studies, designed to correlatehealth effects with fungi count, provided divergentresults (Peat et al. 1998; Douwes and Pearce 2003).Altogether, there is still a lack of information aboutmould levels in homes and whether indoor mouldexposures are related to allergies (Muller et al.2002).Fungi carry allergens (Kurup 2003) against which

the human body develops IgE and IgG antibodies(Nolles et al. 2001), but only a few fungal allergenshave been precisely characterized. In a recent study,the relationship between indoor fungi (spore countin settled house dust) and allergic sensitization inchildren was investigated (Jacob et al. 2002). It wasfound thatmold spore counts forCladosporium andAspergilluswere associatedwith an increased risk ofallergic sensitization.Our preceding cross-sectional study (Landesge-

sundheitsamt 1997) had shown an associationbetween dampness and moulds in homes and theself-reported risk for development of allergies andrespiratory diseases. In order to get more objectiveinformation,we performed the present investigationwith the following characteristics: study time waswinter term to avoid an influences of outdoor fungi,several methods were applied for exposure assess-ment, measurement of mould-specific immunoglo-bulins IgE was included.

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�� The investigation was performed in the frame of a healthsurvey (Piechotowski et al. 1995) in south-west Germanyin two urban industrial regions (Stuttgart,Mannheim), anindustrial area in rural setting (Kehl) and a rural area(Aulendorf/Bad Waldsee) (Figure 1). The study popula-tion were voluntary 4th-graders (age 9 ± 11 years) living inthe study areas. The State Health Agency coordinatedthese investigations and conducted the analyses. The localteams of the four sentinel health departments (medicaldoctor plus assistant) received a training in the StateHealth Agency and proceeded in a standardized manneron the basis of a study manual. The field study in thehomes was carried out between November 1999 andMarch 2000.

�� Altogether 2124 questionnaireswith an information letterwere delivered to the parents of all 4th-graders in the fourstudy areas in September 1999. The history of allergic

conditions of the children was asked in the healthquestionnaire. Children were defined as having an allergiccondition (cases) if the parents answer that the child hasbeen diagnosed by a doctor to suffer from at least one ofthe following allergic disorders during its lifetime: asthma,asthmoid-spastic or obstructive bronchitis, hay fever,atopic eczema.The parents of 1118 children (52.6%) gave a written

informed consent. Out of these, 640 children wererandomly selected for consideration to participate (278cases and 362 controls), and 397 of these (199 cases and198 controls) were finally included in the study.

�� The health questionnaire had been developed on the basisof the questionnaires of the International StudyonAsthmaandAllergies inChildhood (Asher andWeiland1998), andrelated field studies (Mutius et al. 1991; Braun-Fahrl‰n-der et al. 1995). The questionnaire included 65 itemsinvestigating:

� perceived respiratory and allergic symptoms (wheez-ing, breathlessness)

� medical diagnosis of rhinitis, bronchitis, asthma anddermal allergies

� medical follow-up and treatment, including drug con-sumption.

Furthermore, questions about environmental exposures(such as exposure to cigarette smoke, pet ownership),parental history of atopic diseases, educational degree ofparents, number of siblingswere asked. The questionnairewas filled out at home by the parents.

�� A checklist with 49 items was used to obtain informationon type and age of home, size of the dwelling, type of the

�� ! The four investigation areas (dots) of the study

370 S. Jovanovic et al.

heating, signs of dampness, age of carpets and mattresses,tightness of windows, ventilation and cleaning habits inthe home. A trained interviewer completed it in eachdwelling on the sampling day.The homes of the children were inspected for the

presence of visible mould patches. Samples were taken inthe children's bedroom to determine culturable mouldspores in indoor air, outdoor air, household dust fromfloors and mattresses. Temperature and relative humiditywere measured.

�� Data on colony-forming units (CFU/m3) and fungalcomposition in air were obtained using Merck AirSamplers MAS 100. Samplers were equipped with DG18 plates (dichloran-18% glycerol agar). Four sampleswere taken in the center of the children's bedroom at aheight of 50 cm. In addition, four outdoor air sampleswere taken at a distance of 1 m from the window of theroom. Sampling time was adjusted to collect 50 l (2samples) and 100 l (2 samples). The plates were incubatedfor 5 ± 7 days at 28 �C (Jovanovic et al. 2001). In additionfungal colonies were differentiated to genus level bymicroscopy. The abundance of the most common mouldgenera on each plate was recorded using a semiquantita-tive grading scale: 1� rare, 2� common, 3� frequent. Allexaminations and semi-quantifications were done by thesame investigator.

�� Dust samples for analysis of moulds were collected in astandardized manner using a vacuum cleaner with specialfilter holder and gelatin filter (VDI 1999). Areas of 1 m2

were sampled from the floor and from the child's mattressfor 5 min. The mass of dust was determined by weighingthe filter before and after dust sampling. The dust was notsieved. A defined quantity of dust was suspended 1 :100 in0.9%NaCl/TWEEN 80 and dilutions were plated on DG18 (dichloran-18% glycerol agar) andMEA (malt extractagar) and incubated (28 �C, 5 ± 7 days). Quantitative andqualitative identification of mould was done in the sameway as for air samples. Quality aspects (Fischer and Dott2002) were given special attention and an external qualitycontrol system was established (Gabrio et al. 2003).

�� Venous blood samples (5 ml) were taken from 352children for determination of serum IgE against a mixtureof moulds (MX2-Test, Pharmacia with the mixture:Penicillium notatum (chrysogenum), Cladosporium her-barum, Aspergillus fumigatus, Candida albicans, Alter-naria alternata,Helminthosporium halodes). Positive serawere additionally tested for specific IgE against Penicil-lium notatum (chrysogenum) (m1), Cladosporium her-barum (m2), Aspergillus fumigatus (m3) and Alternariaalternata (m6). Measurements were conducted with aradioallergosorbent fluorescence immunoassay (CAP-RAST System, Pharmacia, Freiburg, Germany), with acutting point for positive samples at 0.35 kU/l as recom-mended by the manufacturer.

"��# ��Calculationswere performedwith the statistics package ofSAS (versions 6.08 ± 6.12) in the PC version underWindows (SAS Institute Inc.) For statistical tests an errorrate was generally fixed at ��0.05. Graphics weregenerated with the software Statview.Logistic regression analysis was performed to identify

associations between mould levels and allergic condition,adjusting for questionnaire answers given with regard tohome characteristics, health status and social status.The participation in the study was voluntary. Written

informed consent was given by the parents of all partici-pating children. The evaluation was carried out afteranonymization of the personal data; the examinationdesign was coordinated with the agency for data securityof Baden-W¸rttemberg. The examination program isapproved by the ethics committee of the Medical Councilof Baden-W¸rttemberg.

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Visible mould growth was recorded in 65 children'sbedrooms (16.3%). In 10 homes (6 in Mannheim,3 in Aulendorf/Bad Waldsee, 1 in Kehl) the visiblemould surface was larger than 1 m2. Six of theserooms were in homes of the control group and fourin homes of children with allergic conditions. Theconcentration of mould spores in air and dust (CFU/m3 and CFU/g dust) differed widely among thehomes. The median of mould spores (CFU/m3) inindoor air was 105 (range 5 to 15000), in outdoorair 110 (range 10 to 1500). The median of mouldspores (CFU/g) in floor dust was 28500 (range 1500to 1235000), in mattresses 16250 (range 0 to2500000). There was only a weak correlationbetween total mould counts in floor and mattressdust, for other parameters there was not anycorrelation (Figure 2).A total of 48 mould species were differentiated in

this study. The most common fungal genera occur-ring in air sampleswereAspergillus spp.,Penicilliumspp. and Cladosporium spp. The fungal flora ofmattress dust consisted mainly of Aspergillus spp.andPenicillium spp. The fourmost abundant generaas well as the sum of the others were evaluated in asemiquantitative manner (Figure 3). Statistical ana-lysis for possible influence factors onmold levels andgenera patterns did not showsignificant associationswith any of the housing characteristics (relativehumidity, temperature, visible moulds, carpet,dampness, ventilation). The concentration of fungiin floor and mattress dust correlated significantlywith collected weight of dust. Concerning regionaldifferences, the air samples from Kehl and Man-nheim and dust samples from Kehl showed statisti-

Indoor fungi and allergy in children 371

�� $ Correlation of mould counts in indoor air and outdoor air; data of all investigated households

�� % Fungal spectrum (Asp�Aspergillus spp., Pen� Penicillium spp., Alt�Alternaria spp., Clad�Cladosporium spp.) in indoor air (IA),outdoor air (OA), floor dust (F) and mattresses dust (M). Grading scale for the abundance of mould genera: 1� rare, 2� common, 3�frequent.


cally significant higher mould concentrations thanthose from Aulendorf (Figure 4). However, therewas nodifference in the distributionofmould generalevels.

When we stratified the results for allergic historyof the child, there was no difference in concentra-tions and distribution of mould genera levels be-tween children with and without allergic history

�� & Mould counts and distribution of mould genera in dust samples (mattresses and floor) separated by investigation areas

�� ' Mould counts and distribution of mould genera in dust samples in homes of children with (cases) and without (controls) allergichistory

�� ( Mould counts and distribution of mould genera in homes of children with (positive) and without (negative) sensitization (IgE)against mould allergens


(Figure 5). Likewise, the average amount (median)of house dust sampled in homes of children withallergic history (mattress 398 mg/m2, floor 613 mg/m2) did not differ from that of controls (mattress403 mg/m2, floor 684 mg/m2).More subjects were sensitized to moulds

(MX2 mixture) among the children with allergichistory (9.2%) than among the controls (4.4%).From children sensitized to the MX2 mixture,90.5% were sensitized to Alternaria alternata,33.3% to Aspergillus fumigatus, 33.3% to Clados-porium herbarum and 28.6% to Penicillium nota-tum. There was neither a difference in indoor moldlevels (CFU), nor in indoor fungal spectra betweenthe two groups (Figure 6).

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Indoor mould exposure is discussed as a significantpublic health concern throughout the world, but thenature and extent of the problem arising from livingor working in dump buildings is not clearly known(Garrett et al. 1998; Bornehag et al. 2001). It is notclear whether increased mould levels at home areassociatedwith an increased risk of allergies. Severalstudies with positive findings have relied on self-reported mould exposure (Andriessen et al. 1998;Zock et al. 2002). However, self-reported data mayhave the disadvantage (bias) that atopic families aremore aware of home hygiene and report moremould-contamination than control persons. There-fore it would be desirable to rely on an objectivemeasuring method for indoor mold. Fungal concen-tration and composition of fungal genera have beenreported as good indicator for moisture problems(Hyvarinen et al. 2001).Although inhalable airborn allergens are thought

to be relevant for asthma (Salvaggio 1994; Lopuhaaet al. 2003) the short-term measurement of airbornfungi has been criticized, as it is not representativefor the longtime inhalative exposure (Pasanen2001). As an alternative, mould measurement insettled dust is assumed to reflect long-term exposurebetter than short-term air sampling (Dillon et al.1999), even if dust is also subject to variabilities(Topp et al. 2003).Moreover, fungal concentrationsin dust may be clinically relevant, because dermalcontact of childrenwith house dustmay be a route ofsensitisation. Therefore, the present study measuredfungi levels not only in the air, but also in house dustof the children's rooms. In addition, mattress dustwas measured as potentially relevant exposure

source, since children spend about one third of theday in bed.

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The results on frequencies and compositions offungal flora in indoor air, house dust and bed dustare in good agreement with those described by otherauthors from countries with similar climatic andenvironmental conditions and similar western stylebuildings (Ostrowski 1999; Koch et al. 2000; Op-permann et al. 2001; Shelton et al. 2002).The predominant fungi genera were Aspergillus

and Penicillium, followed by Cladosporium andAlternaria. This is in accordancewith the findings ofother studies in this area (Koch et al. 2000; Opper-mann et al. 2001). Alternaria, which is common inoutdoor air in summer, was comparably low in air,but higher in the dust samples. This is compatiblewith the idea, that floor dust reflects mould deposi-tions in the past, here including summer seasons.Wedid not detect any systematic association betweenmould genus patterns and either total levels ormould patches on the walls.In indoor air, the present study foundanaverage of

105 CFU/m3 , which is similar to 198 CFU/m3 foundin California (Macher et al. 1991) and 189 found inPoland (Lis et al. 1997), but lower than 549 CFU/m3

found in Australia (Dharmage et al. 1999). For floordust, the present study found a median of28500 CFU/g (mean 135207), a Belgian one135586 (median) (Beguin and Nolard 1996), aDutch one 71280 (mean) (Chew et al. 2001) and aCanadian study 255000 (mean) (Dales et al. 1997).Finally, in mattress dust, the average amount ofcultivable mould spores was 16250 CFU/g dust(median) and 38238 (mean), which is in a similarrange as results from Poland (16000; Horak et al.1996) and from the Netherlands (6760 (mean);Verhoeff et al. 1994). These comparisons suggestthat the average fungi exposure levels in southernGerman homes are similar to those found in manyother parts of Europe and the world. All studiesfound large variabilities of fungi levels betweenhomes, with a factor of more than 1000 between theextreme values. Despite the numeric similarities ofcolony counts, the comparisons have to be regardedwith some caution, as sampling procedures andcultivation methods varied between the studies,which can be expected to have an influence onresults (Douwes and Pearce 2003).The virtually missing association between the

levels of airborn fungi and fungi in the house-dust


is in accordance with the literature (Douwes andPearce 2003) and supports the assumption that theamount of whirled-up dust is subject to largevariability. The missing association between fungilevels in mattress dust and house dust is notsurprising, since the mattress forms a deep compart-ment with only restricted exchange with the housedust, especially if it is new.Concentrations of moulds varied hardly between

the four investigation areas, and neither climatolo-gical conditions nor differences between urban andrural regions exhibited a systematic influence.This isin accordance with other studies (Koch et al. 2000),which found no significant difference for total viablefungi and for individual genera of spores in settledhouse dust between two urban regions in Germany(Erfurt and Hamburg).

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At present, there is no conclusive evidence for therole of indoor fungi for allergies in children. Somestudies find an association (Taskinen et al. 1997,2002), others do not (Garrett et al. 1998). Thereseems to be insufficient evidence for the associationof indoor mould with asthma, but indoor mould isassociated with exacerbation of asthma in mould-sensitized patients (NAS 2003).In the present study, we found dampness and

visible moulds slightly more frequently in the roomsof children without allergic condition. Statisticalevaluation with multiple logistic regression modelsdid not show any significant associations betweenthe indoor concentration of moulds (total CFU) inair, house dust or bed and reported allergic condi-tion. This is in agreement with observations of otherauthors (Brunekreef 1992; Ostrowski 1999; Jacobet al. 2002).

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Allergies and asthma are clinical findings that cannot be measured with high accuracy on the basis ofquestionnaires in population-based studies (Gru-challa et al. 2003). Methods that deliver a moreobjective picture of the specific reactivity of the bodyto mold exposure include clinical tests, such as theprick test and bronchial provocation test as well aslaboratory tests, such as histamine release andimmunoglobulins (Nusslein et al. 1987; Resanoet al. 1998; Lander et al. 2001; Immonen et al.

2002).Wemeasured fungi-specific IgE, the presenceof which connotes that exposure to one or morespecies has occurred, but not necessarily that there isa symptomatic clinical state (Bardana 2003). Thesensitization rate of the control children (4.4%) wascomparable to the reactivity of children tomoulds inthe prick test in Finland (5%) (Taskinen et al. 1997).The higher sensitization rate in children with anallergic condition (9.2%) is in accordance with theincreased mould-specific IgE levels (�20%) inselected asthmatic children (Koivikko et al. 1991)or asthmatic adults (Ezeamuzie et al. 2000). Pre-valence of specific IgE for Alternaria ranked first,followed by Aspergillus, Cladosporium and Penicil-lium. This ranking was similar to that found in another study (Nolles et al. 2001)where the prevalenceof specific IgE for Cladosporium ranked first,followed closely by Aspergillus and Alternaria.Despite the fact that children pass about 80% of

their time at home and although IgE is an objectiveparameter, the present study failed to detect anassociation between residential mould levels (air,dust) and IgE levels in the children.Themethods used in this study aimed at collecting

objective information for exposure and allergy (IgE)and delivered valuable information on fungi levels inchildren's rooms. Nevertheless it can not be exclu-ded that in future studies with refined methodology,the missing associations can be found. First, expo-sure was assessed on the basis of single (spot)measurement, which does not necessarily representaverage mould burden of a home (Hyvarinen et al.2001), Second, culturable spores represent only asmall fraction of total airborne moulds and mouldfragments, and do not need to represent the mouldspecies with the major allergenic potential (Chewet al. 2001). Finally, the MX-2 test for studying IgElevels does not necessarily include the most relevantallergens. Thus, despite the negative findings, finalconclusion should not be drawn from the presentoutcome.Considering the ongoingdiscussions (Rosset al. 2000; Kolstad et al. 2002; Douwes and Pearce2003), it appears important that methods for asses-sing fungal sensitivity in children and for identifyingthose mould particles with the highest allergenicpotential are improved (Schweinsberg and Mersch-Sundermann 2003).

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The present study has expanded the knowledge offungi exposure in homes of southern Germany anddefined mould-specific IgE-levels in children. It was


performed according to the state of the art. Theresults of our study lead to the conclusion that withcurrent methods for assessing mould exposure andallergy history it remains difficult or impossible todetermine causality and attributable health risks.Further research on the basic clinical effects of

moulds is needed. The development and validationof clinically useful specific biomarkers of mouldexposure and early biological effects should be apriority. There is also a need for improvement andstandardization in the tools for exposure assessmentof moulds at genus level, fungal antigens, fungalfragments andmetabolites. Prospective longitudinaland intervention studies are required to furtherelucidate the role of fungi in environmental hygieneand allergies.

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Indoor fungi levels in homes of children with and without allergy history