Figures
- FIGURE 1
Adjusted odds ratios (aOR) and 95% confidence intervals for asthma development and wheeze from the meta-analyses. CA: current asthma; E-DA: ever-diagnosed asthma; W: wheeze; A: asthma; MO: mould odour; VM: visible mould; D: dampness.
Tables
- TABLE 1
Exposure to moulds using qualitative metrics and asthma occurrence in children (longitudinal studies)
First author, location [ref.] Study design Mould exposure Main outcomes Results Pekkanen, Finland [98] Cases n=121
Controls n=242Home inspection
Visible dampness and mouldChildren aged 1–7 years
Doctor-diagnosed incident asthmaMain living quarters
Dampness: yes versus no
OR 2.24 (1.25–4.01)
Moulds: yes versus no
OR 2.59 (1.15–5.85)Karvonen, Finland [99] Cohort
n=396Home inspection
Visible mould
and humidity
First 6 months of lifeMother's questionnaire at 2, 12 and 18 months Visible mould: yes versus no
Doctor-diagnosed wheezing
Main living quarters
aOR 3.92 (1.54–10)
Child bedroom
aOR 5.22 (1.48–18.35)Schroer, USA [100] Cohort (CCAPS)
n=570Home inspection
Visible mould
Mould odour
First year of lifeParents’ ISAAC questionnaire
Wheezing at 2 years
Persistent wheezing at 1 and 2 yearsVisible mould: yes versus no
Wheezing at 2 years
aOR 2.12 (1.25–3.60)
Persistent wheezing
aOR 2.47 (1.27–4.80)Dales, Canada [101] Cohort
n=330Home inspection
Visible mould
First year of lifeAcute and upper respiratory events
Birth to 2 yearsVisible mould: yes versus no
nsLarsson, Sweden [102] Cohort
n=4779 childrenSelf-reported visible dampness and mould
Reported mould odour
At birthIncident asthma
at 6–8 years
Parents’ questionnaireMould odour:
OR 2.99 (1.50–5.94)Hwang, Taiwan [103] 1–7 years
Cases n=188
Controls n=376Self-reported mould or mould odour between birth and 1 year Reported doctor- diagnosed incident asthma 6 years later Visible mould: yes versus no
aOR 1.76 (1.18–2.62)
Mould odour: yes versus no
aOR 2.09 (1.30–3.37)
Moulds + parent atopy
aOR 5.10 (2.80–9.31)
Odour + parent atopy
aOR 4.11 (2.22–7.64)Hwang, Taiwan [21] 1–7 years
Cases n=188
Controls n=376Self-reported mould or mould odour between birth and 1 year Reported doctor- diagnosed incident asthma 6 years later + polymorphisms of interleukin-4 promoter Visible mould: yes versus no
CT versus TT polymorphism:
OR 2.14 (1.05–4.34)Zhou, France [23] Cohort
n=1765Self-reported humidity or moulds
First year of lifeISAAC questionnaire
0–4, 4–8 and 8–12 monthsHumidity and diagnosed asthma + wheeze
aOR 2.21 (1.04–4.71)
Wheeze aOR 2.12 (1.30–3.46)
Diagnosed life-time asthma
aOR 2.19 (1.06–4.53)Wen, Taiwan [24] Cohort
n=19 192Visible mould during pregnancy
Health questionnaire at 0.5, 1.5, 3 and 5 yearsEver doctor-diagnosed asthma in 5-year-old children Visible mould: yes versus no
aOR 1.21 (1.01–1.46) Only in femalesShorter, New Zealand [22] Nested incident cases n=150
Controls n=300Bedroom wall (electrostatic dust cloth) for 4 weeks
Visible mould and odourChildren aged 1–7 years
Incident wheezingVisible mould and mould odour in a dose-dependent manner Karvonen, Finland [25] Cohort
n=398Home inspection
Visible mould and humidity
First 6 months of lifeEver physician-diagnosed asthma
≤6 yearsVisible mould: yes versus no
Living room
aOR 7.51 (1.49–37.83)
Child's bedroom
aOR 4.82 (1.29–18.02)
Allergic asthma
aOR 9.08 (1.95–42.23)Thacher, Sweden [26] BAMSE cohort
n=3798Any self-reported mould or dampness indicator (dampness damage, visible mould or mould odour) in infancy (2 months) Asthma ≤16 years Any indicator
Asthma
OR 1.31 (1.08–1.59)
Nonallergic asthma
aOR 1.80 (1.27–2.55)aOR: adjusted odds ratio; CCAPS: Cincinnati Childhood Allergy and Air Pollution Study; ISAAC: International Study of Asthma and Allergies in Childhood; ns: nonsignificant; BAMSE: Barn/Child Allergy Milieu Stockholm Epidemiology.
- TABLE 2
Exposure to moulds and exacerbation of asthma in children (panel studies)
First author, location [ref.] Study design Mould exposure Main outcomes Results Hagmolen of Ten Have, the Netherlands [104] 526 children with asthma (mean age 11 years)
Follow-up: 2 weeks (2 visits)At baseline: positive response to a question on visible mould in the past 2 years Daily variability of peak flow
Daily symptoms: wheezing, cough, BHR at follow-upNo association between mould exposure and symptoms
In exposed children: increased peak flow variability: +2.70% (95% CI 0.92–4.47, p=0.003), and higher BHR: aOR: 3.95 (1.82–8.57)Inal, Turkey [105] 19 children with asthma or rhinitis, and monosensitised to mould (aged 4–13 years)
Follow-up: 1 yearEvery month: indoor air:
MAS-100 Eco 100 L·min−1
Culture CFU·m−3: Cladosporium, Penicillium, Aspergillus, Alternaria and others (undefined or >1%)Daily variability of peak flow: morning and evening
Daily symptoms (rhinitis and asthma scores)No association between mean exposure to mould (37.5 CFU·m−3) and daily variability of peak flow or symptoms Bundy, Western Massachusetts and Connecticut, USA [106] 225 children with asthma (6–12 years old)
Follow-up: 2 weeksAt baseline: indoor air:
Burkard 1 min 20 L·min−1
Culture and classification:
0 CFU·m−3, 1–499 CFU·m−3, 500–999 CFU·m−3, >1000 CFU·m−3, Cladosporium, Alternaria, Penicillium or AspergillusDaily variability of peak flow: three series of measurements morning and evening performed by children
Daily symptoms (wheezing, cough and nocturnal symptoms), drugs reported by the motherNo association between mould exposure and symptoms
Associations between Penicillium (0 versus detectable) and peak flow variability of >18.5% (75th percentile) aOR 2.39 (95% CI 1.19–4.81)Pongracic, the Inner-City Asthma Study: USA
[107]469 children with mild to severe asthma and at least one positive SPT to mould (aged 5–11 years)
Follow-up: 2 yearsAt baseline and every 6 months: indoor air
2 measurements Burkard 1 min 30.5 L·min−1, 1 m from floor, children's room
Outdoor air
Culture CFU·m−3: Cladosporium, Alternaria, Penicillium and Aspergillus
Dust measurements on floor and bedCall report every 2 months:
max number of days (in 2 weeks) with symptoms (wheezing, cough, chest tightness, awakening due to asthma or play activities stopped because of asthma)
Number of unplanned visits to hospital or EV in the past 2 monthsAssociation between 10-fold increase in Penicillium level and increased number of days with symptoms: 1.19 days per 2 weeks, p<0.03
Association between indoor mould and exacerbations and EV:
aOR 1.22 (95% CI 1.05–1.43) and 1.13 (1.01–1.26)
Association between Penicillium and EV:
OR 1.15 (1.05–1.27) (all children), and 1.11 (1.03–1.20) in those SPT− for PenicilliumWu, USA [32] 395 children with mild-to-moderate persistent asthma
CAMP study
(aged 5–12 years)
Follow-up: 6 months and 3 years or before in case of movingAt baseline and at the first follow-up (6 months):
dust measurements on floor (main living room, bedrooms and kitchen) and on child's bed
Vacuum cleaner equipped with a filter (Douglas ReadiVac model): 2 min for each zone of different surfaces
Culture and classification: high mould dust exposure: >25 000 CFU·g−1 of house dustSevere asthma exacerbations
Hospitalisations or urgent care visits during the 4 years of follow-up (report every 4 months)
Polymorphisms (SNPs) in chitinase genes24% (n=95) had high mould dust exposure
Number of urgent care visits increased with high mould dust exposure in children with genetic polymorphisms (rs2486953, rs4950936 and rs1417149) in the CHIT1 geneGent, Western Massachusetts and Connecticut, USA [108] 1233 school-aged children with asthma (aged 5–10 years)
Follow-up: 1 monthAt baseline: indoor air:
Burkard 1 min 20 L·min−1, culture: CFU·m−3
Dust measurements on floor and furniture in the main living room
Blood allergens: mould, mites, cat, dog (µg·g−1) and cockroaches (U·g−1)Daily symptoms (wheezing, cough), drugs and severity (five levels)
Allergic sensitisation: allergens and IgEIn sensitised children: associations between Penicillium and risk of wheezing: aOR 2.12 (95% CI 1.12–4.04), cough: 2.01 (1.05–3.85) and asthma severity score: 1.99 (1.06–3.72) Vicendese, Melbourne, Australia [33] Nested incident case–control study within the MAPCAH study: 44 children (aged 2–17 years)
Follow-up: September 2009 to December 2011Air fungi in the child's bedroom: two-stage Andersen Sampler for 1 min, flow rate: 28 L·min−1
Total fungi, Cladosporium, Penicillium/Aspergillus and Alternaria, CFU per 28 L of airStandardised questionnaires from the ISAAC and NZ Otago studies
Incident asthma readmissionsAssociation between every doubling concentration of CFU of airborne Cladosporium (per 28 L of air) in the bedroom and asthma readmission:
aOR 1.68 (95% CI 1.04–2.72)Dannemiller, Western Massachusetts and Connecticut, USA [34] n=196, subgroup of the 1233 school-aged children with asthma (aged 5–10 years)
Follow-up: 1 monthAt baseline: indoor air: Burkard 1 min 20 L·min−1, culture: CFU·m−3
Dust measurements on floor and furniture in the main living room
Total fungi concentration dichotomised at the median (high and low exposure)Daily symptoms (wheezing, cough), and medication use
Asthma severity (five levels) expressed as mild (reference, 0 or 1) or severe (3 or 4), level 2 not included in the analyses
Total and specific IgEAssociation between high fungal concentration and asthma severity in all children:
aOR 2.02 (95% CI 1.14–3.56) and in nonatopic children:
aOR 2.40 (95% CI 1.06–5.44), but not in atopic children:
1.69 (0.77–3.75)Casas, HITEA project: Spain, the Netherlands, Finland
[35]419 children (aged 6–12 years) from 25 schools: 106 children from 8 schools in Spain, 150 children from 11 schools in the Netherlands, 163 children from 6 schools in Finland
Follow-up: 1 yearSchool with or without (reference) moisture damage: number, extent, severity and location of dampness, and moisture damage observations recorded during inspections Three symptom diaries: a 2-week diary starting before the summer school holiday (May–July 2009), a 3-week diary starting at the end of the summer holiday (August–October 2009) and a 2-week diary during winter and spring (January–May 2010)
16 symptoms in the past 24 h: wheeze, shortness of breath, dry cough during day or at night, phlegm, woken up… and severity (no symptom, slight, moderate or severe)Holiday and weekends were associated with lower scores
Results were heterogeneous across the three countries
In Spain, all adjusted IRRs <1 for summer holiday (ref. school day) in schools with moisture damage: lower respiratory symptoms IRR 0.61 (95% CI 0.46–0.81), upper respiratory or allergy symptoms 0.78 (95% CI 0.63–0.93), other symptoms 0.64 (95% CI 0.49–0.83)
Similar results in Finland for summer holiday and weekend
All random-effect combined IRRs <1HITEA: Health Effects of Indoor Pollutants: Integrating Microbial, Toxicological and Epidemiological Approaches; BHR: bronchial hyperresponsiveness; aOR: adjusted odds ratio; EV: emergency visit; SPT: skin prick test; SNP: single nucleotide polymorphism; Ig: immunoglobulin; MAPCAH: Melbourne Air Pollen Children and Adolescent Health; ISAAC: International Study of Asthma and Allergies in Childhood; IRR: incidence rate ratio.
- TABLE 3
Longitudinal studies on occupational asthma related to working in mouldy buildings
First author, location [ref.] Study design Mould exposure Main outcomes Results Park, USA [46] Nested study
Cases n=49
Controls n=152
Employees working in a water-damaged buildingFloor and chair dust
TCF
HF
Endotoxins
Pet allergensPOA POA (for increasing IQR)
and chair dust
Single environmental variable
aOR (95% CI)
TCF 1.67 (1.07–2.60)
HF 1.85 (1.19–2.89)
Multiple environmental variables:
HF 1.79 (1.12–2.85)Karvala, FIOH: Finland
[42]Patients assessed between 1995 and 2004 for suspicion of mould-induced OA
n=258Retrospective work exposure:
building damage report and microbial analysesSIC with mould extracts, especially A. fumigatus, C. cladosporioides and A. kiliense
Three OA groups: probable, possible, unlikelyMould duration exposure usually >5 years
Sensitisation to moulds:
probable: 20.4%
possible: 10.7%
unlikely: 4.4%
Among 133 probable OA (SIC+):
A. fumigatus: 85
C. cladosporioides: 26
A. kiliense: 19Karvala, FIOH: Finland [43] Longitudinal study over 3–12 years
n=483Exposure:
building damage report and microbial analysesDoctor-diagnosed incident asthma among patients
with ALS related to damp workplaces, but without asthma at baselineDoctor-diagnosed incident asthma
No more exposition (ref.)
Same remediated
OR 2 (95% CI 0.7–5.4)
Persistent exposure:
OR 4.6 (95% CI 1.8–11.6)Park, USA [47] Employees working in a damp building. Baseline
n=131 BR-RS without asthma
n=361 without BR-RS and asthma at baselineFloor dust:
TCF
Ergosterol
EndotoxinsBR-AS development BR-AS development: aOR (95% CI)
BR-RS 1.00 (ref.)
BR-RS+ 2.24 (1.34–3.72)
Baseline TCF
1st tertile 1 (ref.)
2nd tertile 3.59 (1.46–8.83)
3rd tertile: 4.92 (1.90–12.72)Karvala, FIOH: Finland [44] Longitudinal study over 3–12 years
n=1267Exposure: building damage report and microbial analyses Quality of life
SF12 physical and mental component scores
Four baseline groups
n=127 OA
n=453 WEA
n=483 ALS
n=204 URSSF12, physical component score
Mean±sd
URS 69.7±28.9
ALS 62.9±29.7
WEA 54.7±30.6
OA 45.4±29.1
p <0.001Karvala, FIOH: Finland
[45]Longitudinal study over 7–8 years
n=1098Exposure: building damage report and microbial analyses Self-rated work ability
0: low <scale<10: best
Early withdrawal from work owing to disability Four baseline groups
n=127 OA
n=453 WEA
n=483 ALS
n=204 URSLow self-rated work ability (scale <8)
%, aOR (95% CI)
URS 34%, 1.0
ALS 40%, 1.2 (0.8–1.7)
WEA 50%, 1.8 (1.2–2.8)
OA 57%, 2.6 (1.4–4.7)
Early withdrawal from work
%, aOR (95% CI)
URS 7%, 1.0
ALS 13%, 1.6 (0.8–3.1)
WEA 13%, 1.6 (0.8–3.1)
OA 33%, 5.7 (2.8–11.9)FIOH: Finnish Institute of Occupational Health; TCF: total culturable fungi; HF: hydrophilic fungi; POA: post-occupancy asthma; IQR: interquartile range; aOR: adjusted odds ratio; OA: occupational asthma; SIC: specific inhalation challenge; A. fumigatus: Aspergillus fumigatus; C. cladosporioides: Cladosporium cladosporioides; A. kiliense: Acremonium kiliense; ALS: asthma-like symptoms; BR: building-related; RS: rhinosinusitis; AS: asthma symptoms, WEA: work-exacerbated asthma; URS: upper respiratory symptoms; SF12: 12-item short form survey.
- TABLE 4
Mould exposure and rhinitis: findings from meta-analyses, longitudinal studies and birth cohorts
First author [ref.] Study design Mould exposure Main outcomes# Results Fisk [15] Meta-analysis
13 cross-sectional + longitudinal studies
Children and adultsDampness and/or mould Upper respiratory tract symptoms OR 1.70 (95% CI 1.44–2.00) Antova [5] Pooled analysis of seven cross-sectional studies as part of the PATY study
Children aged 6–12 yearsVisible mould Hay fever OR 1.35 (95% CI 1.18–1.53)
p-value from test for between-country heterogeneity p=0.20Tischer [7] Meta-analysis
11 cross-sectional + longitudinal studies
ChildrenVisible mould Allergic rhinitis or hay fever OR 1.39 (95% CI 1.28–1.51) Tischer [8] Pooled analysis of six birth cohorts as part of the ENRIECO initiative Early exposure to mould Allergic rhinitis In early school age (6–8 years)
aOR 1.12 (95% CI 1.02–1.23)
In childhood (3–10 years)
aOR 1.18 (95% CI 1.09–1.28)
No significant heterogeneity between the cohortsJaakkola [48] Cross-sectional, case–control and cohort studies in children or adults
(31 studies overall)Water damage, dampness, visible mould and mould odour Allergic rhinitis EE (95% CI)
Dampness:
(6 studies) mild heterogeneity
1.50 (1.38–1.62)
All EEs >1; 6/6 EEs significant
Visible mould:
(12 studies) no heterogeneity
1.51 (1.39–1.64)
All EEs >1; 6/12 EEs significant
Mould odour:
(3 studies) strong heterogeneity
1.87 (0.95–3.68)
All EEs >1; 2/3 EEs significantBiagini, USA [109] Birth cohort (CCAPS) with at least one parent with positive SPT
n=495 infants with SPT at the age of 1 yearVisible mould during home visit URTI (sinus or ear infection and antibiotic use) reported in diary
Allergic rhinitis = rhinitis symptoms + at least one positive SPTVisible mould:
aOR (95% CI) for URTI (versus ref.= no visible mould)
Low 1.5 (1.01–2.3)
High 5.1 (2.2–12.0)
aOR (95% CI) for allergic rhinitis
Low 1.2 (0.6–2.5)
High 3.2 (0.7–14.8)Osborne, USA [110] Birth cohort (CCAPS) with at least one parent with positive SPT
n=144 children aged 1–3 yearsLong-term air sampling and total fungal spore enumeration in the 8 months around clinical examination SPT to two food allergens and 15 aeroallergens
Questionnaire for parents on rhinitis (sneezing, runny or stuffy nose, when you did not have a cold?)Positive associations between rhinitis and: total concentration (p=0.10), Ganoderma (p=0.06), basidiospores (p=0.01)
Negative associations between rhinitis and: Alternaria (p=0.10)
Positive associations between positive SPT and Alternaria (p=0.01), Penicillium/Aspergillus type (p=0.01)
Negative associations between positive SPT and Ganoderma (p=0.10), basidiospores (p=0.09) and Cladosporium (p=0.04)Inal, Turkey [105] 19 children aged 4–13 years with asthma or rhinitis, and monosensitised to mould
Follow-up 1 yearMonthly sampling of indoor air Daily symptom score of rhinitis in diary No association between exposure to mould (total or Cladosporium, Alternaria, Penicillium or Aspergillus concentration CFU·m−3) and daily symptom score Jaakkola, Finland [111] Population-based prospective cohort
n=1863 children aged 1–7 years, free of allergic rhinitis at baseline in 1991
(n=246 incident cases)Visible mould, wet spots, water damage and indicator of “any” exposure Development of allergic rhinitis (incident cases) (history of or current physician-diagnosed allergic rhinitis during the 6-year follow-up period) OR for allergic rhinitis incidence (compared to ref=no exposure)
Visible mould at baseline 1.06 (0.51–2.21);
at follow-up 1.98 (1.32–2.99)
Mould odour at baseline 0.94 (0.36–2.45);
at follow-up 1.45 (0.89–2.37)
Any exposure at baseline 1.55 (1.10–2.18);
at follow-up 1.62 (1.21–2.18);
at baseline and follow-up 1.96 (1.29–2.98)Behbod, USA [28] Prospective birth cohort
408 children with family history of allergic disease or asthma followed-up to age 13 yearsParental report of home dampness and culturable fungi in bedroom air and dust, and in outdoor air when children were aged 2–3 months Indoor air: Burkard DG18: 1 min 45 L·min−1 Culture: identification of fungal genus Symptoms/disease onset from birth to age 13 years
For rhinitis: parental report of physician-diagnosed hay fever and nasal symptoms (runny nose)
Mould sensitisation status tested at ages 7 and 13 years (in n=285)HR (95% CI) for rhinitis onset
Home dampness 1.11 (0.73–1.68)
Dust (bedroom floor)
Alternaria 0.79 (0.51–1.22)
Cladosporium 0.91 (0.77–1.08)
Aspergillus 1.39 (1.11–1.74)
Penicillium 1.04 (0.89–1.21)
Yeasts 1.06 (0.92–1.22)
Nonsporulating fungi 1.05 (0.88–1.25)
Measures in indoor air: no significant association observedThacher, Sweden [26] Birth cohort (BAMSE)
n=3798 children with follow-up data at age 16 yearsParental report when the child was 2 months, of mould odour ever in the home, visible mould in the home in the past year or moisture damage in the home Rhinitis: eye or nose symptoms following exposure to allergens in the past 12 months and/or a doctor's diagnosis of allergic rhinitis (+/- positive Phadiatop test) at age 16 years OR (95% CI) for rhinitis at age 16 years
Visible mould 1.28 (1.04–1.58)
Mould odour 1.29 (1.03–1.62)
Any mould or dampness indicator for nonallergic rhinitis 1.41 (1.03–1.93);
allergic rhinitis 0.88 (0.74–1.05)PATY: Pollution and the Young; ENRIECO: Environmental Health Risks in European Birth Cohorts; aOR: adjusted odds ratio; EE: effect estimate; CCAPS: Cincinnati Childhood Allergy and Air Pollution Study; SPT: skin prick test; URTI: upper respiratory tract infection; BAMSE: Barn/Child Allergy Milieu Stockholm Epidemiology. #: other outcomes are considered in the articles cited.
Supplementary Material
Please note: supplementary material is not edited by the Editorial Office, and is uploaded as it has been supplied by the author.
Online_supplementary_material ERR-0137-2017_Online_supplementary_material
FigureE1 err-0137-2017-FigureE1
Vol 27 Issue 148
Table of Contents
Indoor mould exposure, asthma and rhinitis: findings from systematic reviews and recent longitudinal studies
