Exposure assessment of residential mould, fungi and microbial components in relation to children's health: Achievements and challenges

doi:10.1016/j.ijheh.2012.05.002

International Journal of Hygiene and Environmental Health

Volume 216, Issue 2, March 2013, Pages 109-114

https://doi.org/10.1016/j.ijheh.2012.05.002 Get rights and content

Abstract

Each day we are exposed to a complex mixture of microbial agents and components in indoor environments. A major part of this mixture derives from fungal and bacterial origin. The impact between those microbial agents in the home environment in relation to respiratory health in children is still a major issue in research. There is little known about the causal agents that provoke or arrest the development of allergic respiratory disorders in children. Identification is complicated by the biodiversity and variability of microbial components in indoor air as well as the lack of validated and standardized exposure assessment methods. In this review, we aim to consider all important aspects in terms of research which may encounter an epidemiological study. Apart from the need for standardized exposure assessment methods which consider cost, handling and effort, especially for the participants, we suggest that a combination of different analysis methods such as chemical and molecular methods may have the potential to best describe the microbial milieu in indoor environments at present. Further, the impact of mould and moisture remediation activities on health is still heavily under investigated, especially in larger prospective cohorts of children and should be a topic of future research. Moreover, the exposure to mould and microbial agents might be embedded in a broader spectrum of children's health such as behavior and cognitive development.

Introduction

Each day we are exposed to a complex mixture of microbial agents and components in indoor environments. A major part of this mixture derives from fungal, bacterial and viral origin (Nevalainen and Seuri, 2005). The impact between those microbial agents in the home environment in relation to respiratory health in children is still a major issue in research (WHO, 2009). There are a number of publications addressing more or less the same research questions such as exposure to fungal or bacterial agents in relation to respiratory and allergic health outcomes (for a review see Mendell et al., 2011). However, the research approaches can vary considerably in some cases which might be partly responsible for inconsistencies found in results (Tischer et al., 2011a).

Previous reviews focused mainly on summarizing exposure–response relationships (Fisk et al., 2007). We focus here on exposure assessment and analysis methods of mould and microbial agents, in addition to the summary of health effects. We aim to consider several important aspects of an epidemiological study such as the impact of different types of fungal and bacterial exposure and different assessment and analysis strategies. We further discuss findings from interventional studies on fungi removal and considered the potential relevance of gene–environment interactions. This work is focusing on what achievements has been made so far in terms of epidemiological research on mould exposure with emphasis on children and further, what are the future challenges and possible research directions concerning mould and microbial pollution in indoor environments.

Section snippets

Exposure to fungal and bacterial agents

Fungi and fungal components are natural and ubiquitous in indoor environments (Green et al., 2006). In ‘healthy’ indoor environments the predominant fungi are the outdoor air genera Cladosporium, Penicillium and Aspergillus (Nevalainen and Seuri, 2005, Jones et al., 2011). However, the presence of dampness or visible mould shifts the composition of the fungal profile toward ‘indicator organisms’ – species such as Penicillium chrysogenum, Penicillium expansum, Aspergillus versicolor, Aspergillus

Health effects of domestic mould and bacterial agents

Available data suggested 20% of the homes worldwide have dampness problems or visible mould (IOM, 2004). A large body of literature supports an association between living in a damp and mouldy environment and adverse respiratory and allergic health disorders in children throughout the world (IOM, 2004, Fisk et al., 2007, Seltzer and Fedoruk, 2007, WHO, 2009, Tischer et al., 2011a, Tischer et al., 2011b). However, being exposed to increased levels of bacteria and mould derived components early in

Assessment of mould and microbial agents

Apart from the difficulty of disentangling the impact of various microbial agents indoors, there is currently no standardised and valid exposure assessment method to measure exposure to microbial agents. Numerous strategies have been used to assess visible mould and microbial exposure in indoor environments in the past (Table 1).

The choice of specific exposure assessment method and the analysis method can significantly impact the interpretation of study findings. One common, simpler approach

Evidence from intervention studies on mould and fungi removal

Recent reviews on housing intervention and the World Health Organization (WHO) guidelines for indoor air quality concluded that there is sufficient evidence for reducing respiratory symptoms after remediation activities, however, this concerns mainly an adult population (WHO, 2009, Jacobs et al., 2010, Krieger et al., 2010, Rao and Phipatanakul, 2011). There is less knowledge about interventional trials on mould remediation in relation to allergic disorders in children. One prospective,

Gene–environment interactions

Apart from the complexity of the exposure, the development of allergic diseases is also based on a complex interplay between environmental and genetic factors. There are a number of genes associated with the development of asthma and allergies in genome wide association studies (Meyers, 2010, Moffatt et al., 2010). Mutations in the toll-like receptor (TLR) pathway genes, especially TLR 4 which is the major signalling receptor for lipopolysacchardies (LPS), were found to alter the response to

Conclusion and recommendations

Dampness and moisture damage is not only an important precondition for mould growth, but also favours the spread of bacterial and other microbial agents. In order to identify patterns of agents evoking harmful or protective effects on the development of asthma and allergic diseases, the focus should be on elaborated assessment and analyses techniques. Up to now, there is no standardised exposure assessment method which would help to better compare results from different studies, to detect

References (84)

R.K. Bush et al.
The role and abatement of fungal allergens in allergic diseases
J. Allergy Clin. Immunol.
(2001)
R.K. Bush et al.
The medical effects of mold exposure
J. Allergy Clin. Immunol.
(2006)
W.W. Busse et al.
Role of viral respiratory infections in asthma and asthma exacerbations
Lancet
(2010)
J.P. Cabral
Can we use indoor fungi as bioindicators of indoor air quality? Historical perspectives and open questions
Sci. Total Environ.
(2010)
J. Douwes et al.
Fungal extracellular polysaccharides in house dust as a marker for exposure to fungi: relations with culturable fungi, reported home dampness, and respiratory symptoms
J. Allergy Clin. Immunol.
(1999)
J. Douwes et al.
Does early indoor microbial exposure reduce the risk of asthma? The prevention and incidence of asthma and mite allergy birth cohort study
J. Allergy Clin. Immunol.
(2006)
M.J. Ege et al.
Not all farming environments protect against the development of asthma and wheeze in children
J. Allergy Clin. Immunol.
(2007)
M.E. Giovannangelo et al.
Levels and determinants of beta(1→3)-glucans and fungal extracellular polysaccharides in house dust of (pre-)school children in three European countries
Environ. Int.
(2007)
Y.Y. Iossifova et al.
Mold exposure during infancy as a predictor of potential asthma development
Ann. Allergy Asthma Immunol.
(2009)
W. Jedrychowski et al.
Cognitive function of 6-year-old children exposed to mold-contaminated homes in early postnatal period. Prospective birth cohort study in Poland
Physiol. Behav.
(2011)

S. Jovanovic et al.

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

Int. J. Hyg. Environ. Health

(2004)

Y.L. Lee et al.

The association between glutathione S-transferase P1, M1 polymorphisms and asthma in Taiwanese schoolchildren

Chest

(2005)

A.H. Liu

Endotoxin exposure in allergy and asthma: reconciling a paradox

J. Allergy Clin. Immunol.

(2002)

A.H. Liu

Something old, something new: indoor endotoxin, allergens and asthma

Paediatr. Respir. Rev.

(2004)

D.A. Meyers

Genetics of asthma and allergy: what have we learned?

J. Allergy Clin. Immunol.

(2010)

A. Muller et al.

Increased incidence of allergic sensitisation and respiratory diseases due to mould exposure: results of the Leipzig Allergy Risk children Study (LARS)

Int. J. Hyg. Environ. Health

(2002)

T. Reponen et al.

Fungal fragments in moldy houses: a field study in homes in New Orleans and Southern Ohio

Atmos. Environ.

(2007)

T. Reponen et al.

Visually observed mold and moldy odor versus quantitatively measured microbial exposure in homes

Sci. Total Environ.

(2010)

J.M. Seltzer et al.

Health effects of mold in children

Pediatr. Clin. North Am.

(2007)

E. von Mutius

Allergies, infections and the hygiene hypothesis – the epidemiological evidence

Immunobiology

(2007)

M. Werner et al.

TLR4 gene variants modify endotoxin effects on asthma

J. Allergy Clin. Immunol.

(2003)

W. Bischof et al.

Predictors of high endotoxin concentrations in the settled dust of German homes

Indoor Air

(2002)

C.G. Bornehag et al.

Dampness in buildings and health (DBH): report from an ongoing epidemiological investigation on the association between indoor environmental factors and health effects among children in Sweden

Indoor Air

(2004)

C. Braun-Fahrlander et al.

Environmental exposure to endotoxin and its relation to asthma in school-age children

N. Engl. J. Med.

(2002)

G.L. Chew et al.

Fungal extracellular polysaccharides, beta (1→3)-glucans and culturable fungi in repeated sampling of house dust

Indoor Air

(2001)

J. Douwes

(1→3)-beta-d-Glucans and respiratory health: a review of the scientific evidence

Indoor Air

(2005)

J. Douwes et al.

Does environmental endotoxin exposure prevent asthma?

Thorax

(2002)

J. Douwes et al.

(1→3)-beta-d-Glucan and endotoxin in house dust and peak flow variability in children

Am. J. Respir. Crit Care Med.

(2000)

M.J. Ege et al.

Exposure to environmental microorganisms and childhood asthma

N. Engl. J. Med.

(2011)

L.H. Engman et al.

How valid are parents’ questionnaire responses regarding building characteristics, mouldy odour, and signs of moisture problems in Swedish homes?

Scand. J. Public Health

(2007)

W.J. Fisk et al.

Meta-analyses of the associations of respiratory health effects with dampness and mold in homes

Indoor Air

(2007)

U. Gehring et al.

House dust endotoxin and allergic sensitization in children

Am. J. Respir. Crit Care Med.

(2002)

U. Gehring et al.

Bacteria and mould components in house dust and children's allergic sensitisation

Eur. Respir. J.

(2007)

J.F. Gent et al.

Levels of household mold associated with respiratory symptoms in the first year of life in a cohort at risk for asthma

Environ. Health Perspect.

(2002)

R.L. Gorny et al.

Fungal fragments as indoor air biocontaminants

Appl. Environ. Microbiol.

(2002)

B.J. Green et al.

Airborne fungal fragments and allergenicity

Med. Mycol.

(2006)

J. Heinrich et al.

Pets and vermin are associated with high endotoxin levels in house dust

Clin. Exp. Allergy

(2001)

J. Heinrich et al.

Reproducibility of allergen, endotoxin and fungi measurements in the indoor environment

J. Expo. Anal. Environ. Epidemiol.

(2003)

K. Huttunen et al.

Production of proinflammatory mediators by indoor air bacteria and fungal spores in mouse and human cell lines

Environ. Health Perspect.

(2003)

K. Huttunen et al.

Comparison of mycobacteria-induced cytotoxicity and inflammatory responses in human and mouse cell lines

Inhal. Toxicol.

(2001)

A. Hyvarinen et al.

Dust sampling methods for endotoxin – an essential, but underestimated issue

Indoor Air

(2006)

A. Hyvarinen et al.

Characterizing microbial exposure with ergosterol, 3-hydroxy fatty acids, and viable microbes in house dust: determinants and association with childhood asthma

Arch. Environ. Occup. Health

(2006)

Cited by (51)

Effects of climate variability on respiratory diseases in the Western Region of Bahia, Brazil
2023, Public Health
This study aimed to analyse hospitalisations for respiratory diseases in the Western Region of Bahia, Northeast Brazil, from 2010 to 2019, and to explore possible correlations with meteorological data.
This descriptive, epidemiological, ecological study analysed data from 37 municipalities in the Western Bahia health macro-region, defined according to geographical, administrative, demographic, epidemiological, social and cultural criteria, and accounting for availability of health resources.
Hospitalisation data for respiratory diseases, including total admissions and disease frequency, mean and prevalence, were obtained from DATASUS (Ministry of Health). The data were evaluated by sex, age group and city. Statistical tests, such as the Chi-squared test and analysis of variance, were used for data analysis. Meteorological data were compared using the t-test and Mann–Whitney test. Correlations between health indicators and weather data were assessed using the Pearson and Spearman correlation coefficients.
Over the investigated period, there were 536,195 hospitalisation records in the region, with respiratory diseases accounting for 17.1% of admissions. Notably, 40% of respiratory hospitalisations were among children aged 0–9 years. The most prevalent respiratory conditions were pneumonia and asthma, which together constituted 73% of all respiratory hospitalisations. A significant negative correlation was observed between respiratory diseases and rainfall (r = −0.70, P = 0.011).
Pneumonia and asthma remain important causes of hospitalisation among children in the Western Bahia Region. The study findings suggest that respiratory diseases are influenced by rainfall, possibly due to increased atmospheric pollutants during time of low rainfall. These findings emphasise the importance of environmental factors in the development and exacerbation of respiratory diseases.
Airborne fungi and human exposure in different areas of composting facilities
2022, Ecotoxicology and Environmental Safety
Airborne fungi can pose serious health concerns in humans; however, the area-specific abundance and composition of airborne fungal microbiota discharged from composting facilities remain unclear. In the present study, we collected air samples from composting, packaging, office, and downwind areas of four commercial composting facilities. The characteristics of airborne fungi, including pathogen/allergen-containing genera, and their corresponding human exposure in different areas of composting facilities were analyzed using high-throughput sequencing and ddPCR. High fungal concentrations and richness were detected in the air of the packaging area. In all four areas, Ascomycota, Basidiomycota, and Mucoromycota were observed to be the primary fungal phyla, with Cladosporium, Alternaria, and Aspergillus as the consistently dominant fungal genera. A large number of endemic airborne fungi were found in the composting and packaging areas, which also shared the most common airborne fungi as well as pathogen/allergen-containing genera. The packaging area contributed substantially to airborne fungi in the office and downwind areas. Area-specific human exposure to broad airborne fungal compositions was revealed, especially regarding the pathogen/allergen-containing genera. Current results provide valuable data for a comprehensive understanding of area-specific airborne fungi in composting facilities and highlight the importance of assessing the inhaled exposure to airborne fungi in evaluating their following health risks.
Airborne bacterial and fungal concentrations and fungal diversity in bedrooms of infant twins under 1 year of age living in Porto
2022, Environmental Research
Citation Excerpt :
In Portugal, the existing legislation for commercial and service buildings (Portaria n.o 353-A/2013 de 4 de dezembro, 2013) includes recommendation on the limit values for airborne bacterial and fungal levels as relevant indoor air quality (IAQ) indicators. It has been established that, in healthy buildings, indoor fungal concentrations should be lower than outdoors (Portaria n.o 353-A/2013 de 4 de dezembro, 2013), since the predominant fungi, including Cladosporium, Penicillium, Aspergillus and Alternaria genera and yeasts, have their main sources outdoors (Cabral, 2010; Tischer and Heinrich, 2013). These fungal genera can constitute sources of potentially hazardous components as allergens, volatile organic compounds (VOC) and mycotoxins to indoor air (Cabral, 2010; Gabriel et al., 2015).
Exposure to airborne microorganisms has been linked to the development of health detriments, particularly in children. Microbial pollution can constitute a relevant health concern indoors, where levels of airborne microorganisms may be specially increased. This work aimed to characterize the airborne bacterial levels, and fungal concentration and diversity to which twins are exposed in their bedrooms (n = 30) during the first year of life. Bacterial and fungal levels varied widely across the studied bedrooms, with 10% of the rooms presenting values exceeding the national limit for both indoor bacterial and fungal counts. Cladosporium was the predominant genera, but Penicillium, Aspergillus, Alternaria, Trichoderma and Chrysonilia were also identified in the samples collected. In addition, two toxicogenic species, A. flavus and T. viride, were identified at counts that exceeded the established limit (12 CFU/m³) in 3 and 7% of the bedrooms surveyed, respectively. Based on indoor-to-outdoor concentration ratios, outdoor air seemed to be the main contributor to the total load of fungi found indoors, while airborne bacteria appeared to be mainly linked to indoor sources. Higher indoor nitrogen dioxide levels were negatively correlated with indoor fungi concentrations, whereas particulate matter and volatile organic compounds concentrations were associated with an increase in fungal prevalence. In addition, rooms with small carpets or located near outdoor agriculture sources presented significantly greater total fungal concentrations. Multiple linear regression models showed that outdoor levels were the single significant predictor identified, explaining 38.6 and 53.6% of the Cladosporium sp. and total fungi counts, respectively. The results also suggest the existence of additional factors contributing to airborne biologicals load in infants’ bedrooms that deserve further investigation. Findings stress the need for investigating the existence of declared interactive effects between chemical and biological air pollutants to accurately understand the health risk that the assessed levels can represent to infants.
Residential bacteria and fungi identified by high-throughput sequencing and childhood respiratory health
2022, Environmental Research
The objective of this study was to examine and compare environmental microbiota from dust and children's respiratory health outcomes at ages seven and twelve.
At age seven, in-home visits were conducted for children enrolled in the Cincinnati Childhood Allergy and Air Pollution Study (CCAAPS). Floor dust was collected and analyzed for bacterial (16 S rRNA gene) and fungal (internal transcribed spacer region) microbiota. Respiratory outcomes, including physician-diagnosed asthma, wheeze, rhinitis, and aeroallergen sensitivity were assessed by physical examination and caregiver-report at ages seven and twelve. The associations between dust microbiota and respiratory outcomes were evaluated using Permanova, DESeq, and weighted quantile sum (WQS) regression models. Four types of WQS regression models were run to identify mixtures of fungi or bacteria that were associated with the absence or presence of health outcomes.
For alpha or beta diversity of fungi and bacteria, no significant associations were found with respiratory health outcomes. DESeq identified specific bacterial and fungal indicator taxa that were higher or lower with the presence of different health outcomes. Most individual indicator fungal species were lower with asthma and wheeze and higher with aeroallergen positivity and rhinitis, whereas bacterial data was less consistent. WQS regression models demonstrated that a combination of species might influence health outcomes. Several heavily weighted species had a strong influence on the models, and therefore, created a microbial community that was associated with the absence or presence of asthma, wheeze, rhinitis, and aeroallergen+. Weights for specific species within WQS regression models supported indicator taxa findings.
Health outcomes might be more influenced by the composition of a complex mixture of bacterial and fungal species in the indoor environment than by the absence or presence of individual species. This study demonstrates that WQS is a useful tool in evaluating mixtures in relation to potential health effects.
Investigation of fungal contamination in urban houses with children in six major Chinese cities: Genus and concentration characteristics
2021, Building and Environment
Indoor fungi, as an important group of biological contaminants, are recognized as risk factors for human health. However, limited data are currently available on fungal pollution in houses of China. In this study, fungi in air, in settled dust and on surfaces in urban houses with children are determined in six major cities of China. Aspergillus spp., Penicillium spp. and Cladosporium spp. are the most frequent genera and are the dominant genera in air. The concentrations of these three fungi account for an average percentage of 87% and 83% of the total concentration of airborne fungi in winter and summer. Unlike airborne fungi, there is no particularly obvious dominant fungal genus in settled dusts and on interior surfaces. The average concentration of total airborne fungi in houses in summer is significantly higher (p < 0.001) than that in winter. In terms of total concentration of airborne fungi, indoor sources significantly contribute to indoor airborne fungi in winter, whereas the contribution of outdoor sources is relatively greater in summer. Average concentration of airborne fungi in northern houses is higher than that in southern houses in both summer and winter. Fungal concentrations in air, in settled dust and on interior surface do not show a strong relationship (r < 0.5), thus air, dust and surface sampling may be all essential to evaluate indoor fungal exposure. The findings of this study are favorable for understanding fungal exposure in houses and can provide bases for establishing control strategies for indoor fungi in China.
Next-Generation sequencing in environmental mycology. A useful tool?
2021, Encyclopedia of Mycology
Fungal spores are ubiquitous in the air and their diversity and quantity vary depending on growth, the geographical location, environmental conditions, and the presence of sources. The health effects linked to this exposure are likely underestimated due to the presence of undocumented fungi. Culture methods are still widely used to describe fungal aerosols. However, there are inherent biases associated with these methods when applied to fungal diversity analyses because most fungal species are difficult to isolate from culture. High-throughput sequencing (HTS) is a good alternative for getting around the non-viable/non-culturable limits of the commonly used methods. In this article, the utility of HTS methods in environmental mycology is discussed from a methodological and a practical point of view to help build a better database on occupational exposure. The comparison of culture and molecular methods is also mentioned to emphasize on the complementarity of both approaches in mycology. Concrete examples of studies successfully using HTS to describe fungal diversity in different environments are also acknowledged. Finally, we present an overview of the different bioinformatic tools and methods required for an accurate analyses of fungal diversity. It illustrates and promotes the use of selected bioinformatic tools in the study of bioaerosols and serves as a good source for learning the “dos and don’ts” involved in conducting a precise microbial ecology study.

View all citing articles on Scopus

View full text

Mini-ReviewExposure assessment of residential mould, fungi and microbial components in relation to children's health: Achievements and challenges

Abstract

Introduction

Section snippets

Exposure to fungal and bacterial agents

Health effects of domestic mould and bacterial agents

Assessment of mould and microbial agents

Evidence from intervention studies on mould and fungi removal

Gene–environment interactions

Conclusion and recommendations

J. Allergy Clin. Immunol.

J. Allergy Clin. Immunol.

Lancet

Sci. Total Environ.

J. Allergy Clin. Immunol.

J. Allergy Clin. Immunol.

J. Allergy Clin. Immunol.

Environ. Int.

Ann. Allergy Asthma Immunol.

Physiol. Behav.

Int. J. Hyg. Environ. Health

Chest

J. Allergy Clin. Immunol.

Paediatr. Respir. Rev.

J. Allergy Clin. Immunol.

Int. J. Hyg. Environ. Health

Atmos. Environ.

Sci. Total Environ.

Pediatr. Clin. North Am.

Immunobiology

J. Allergy Clin. Immunol.

Predictors of high endotoxin concentrations in the settled dust of German homes

Indoor Air

Dampness in buildings and health (DBH): report from an ongoing epidemiological investigation on the association between indoor environmental factors and health effects among children in Sweden

Indoor Air

Environmental exposure to endotoxin and its relation to asthma in school-age children

N. Engl. J. Med.

Fungal extracellular polysaccharides, beta (1→3)-glucans and culturable fungi in repeated sampling of house dust

Indoor Air

(1→3)-beta-d-Glucans and respiratory health: a review of the scientific evidence

Indoor Air

Does environmental endotoxin exposure prevent asthma?

Thorax

(1→3)-beta-d-Glucan and endotoxin in house dust and peak flow variability in children

Am. J. Respir. Crit Care Med.

Exposure to environmental microorganisms and childhood asthma

N. Engl. J. Med.

How valid are parents’ questionnaire responses regarding building characteristics, mouldy odour, and signs of moisture problems in Swedish homes?

Scand. J. Public Health

Meta-analyses of the associations of respiratory health effects with dampness and mold in homes

Indoor Air

House dust endotoxin and allergic sensitization in children

Am. J. Respir. Crit Care Med.

Bacteria and mould components in house dust and children's allergic sensitisation

Eur. Respir. J.

Levels of household mold associated with respiratory symptoms in the first year of life in a cohort at risk for asthma

Environ. Health Perspect.

Fungal fragments as indoor air biocontaminants

Appl. Environ. Microbiol.

Airborne fungal fragments and allergenicity

Med. Mycol.

Pets and vermin are associated with high endotoxin levels in house dust

Clin. Exp. Allergy

Reproducibility of allergen, endotoxin and fungi measurements in the indoor environment

J. Expo. Anal. Environ. Epidemiol.

Production of proinflammatory mediators by indoor air bacteria and fungal spores in mouse and human cell lines

Environ. Health Perspect.

Comparison of mycobacteria-induced cytotoxicity and inflammatory responses in human and mouse cell lines

Inhal. Toxicol.

Dust sampling methods for endotoxin – an essential, but underestimated issue

Indoor Air

Characterizing microbial exposure with ergosterol, 3-hydroxy fatty acids, and viable microbes in house dust: determinants and association with childhood asthma

Arch. Environ. Occup. Health

Mini-Review
Exposure assessment of residential mould, fungi and microbial components in relation to children's health: Achievements and challenges