Health Effects of Moldy Buildings – Microbial Activity

 

This page lists medical journal articles discussing the activity of mold and other microbes in indoor environments.

The Health Effects of Moldy Buildings page of the Paradigm Change site provides further information on this topic.

 

Aleksic B, Draghi M, Ritoux S, Bailly S, Lacroix M, Oswald IP, Bailly JD, Robine E. Aerosolization of mycotoxins after growth of toxinogenic fungi on wallpaper. Appl Environ Microbiol. 2017 Jun 23. PMID: 28646113

This study investigated the mycotoxin production by Penicillium brevicompactum, Aspergillus versicolor and Stachybotrys chartarum during their growth on wallpaper and the possible subsequent aerosolization of produced mycotoxins from contaminated substrates. We demonstrated that mycophenolic acid, sterigmatocystin and macrocyclic trichothecenes (sum of 4 major compounds) could be produced at levels of 1.8, 112.1 and 27.8 mg/m2, respectively on wallpaper. Moreover, part of the produced toxins could be aerosolized from substrate. The propensity to aerosolization differed according to the fungal species. Thus, particles were aerosolized from wallpaper contaminated with P. brevicompactum when air velocity of just 0.3 m/s was applied, where S. chartarum required air velocity of 5.9 m/s. A versicolor was intermediate since aerosolization occurred under air velocity of 2 m/s.Quantification of the toxic content revealed that toxic load was mostly associated with particles of size equal or higher of 3 μm, which may correspond to spores. However, some macrocyclic trichothecenes (especially satratoxin H and verrucarin J) can also be found on smaller particles that can penetrate deeply in the respiratory tract upon inhalation. These elements are important for risk assessment related to mouldy environments.

 

Jančič S, Frisvad JC, Kocev D, Gostinčar C, Džeroski S, Gunde-Cimerman N. Production of Secondary Metabolites in Extreme Environments: Food- and Airborne Wallemia spp. Produce Toxic Metabolites at Hypersaline Conditions. PLoS One. 2016 Dec 30;11(12):e0169116. PMID: 28036382

The food- and airborne fungal genus Wallemia comprises seven xerophilic and halophilic species: W. sebi, W. mellicola, W. canadensis, W. tropicalis, W. muriae, W. hederae and W. ichthyophaga. All listed species are adapted to low water activity and can contaminate food preserved with high amounts of salt or sugar. In relation to food safety, the effect of high salt and sugar concentrations on the production of secondary metabolites by this toxigenic fungus was investigated. Mass spectrometric analysis of selected extracts revealed that NaCl in the medium affects the production of some compounds with substantial biological activities (wallimidione, walleminol, walleminone, UCA 1064-A and UCA 1064-B). In particular an increase in NaCl concentration from 5% to 15% in the growth media increased the production of the toxic metabolites wallimidione, walleminol and walleminone.

 

Piontek M, Łuszczyńska K, Lechów H. Occurrence of the Toxin-Producing Aspergillus versicolor Tiraboschi in Residential Buildings. Int J Environ Res Public Health. 2016 Aug 31;13(9). pii: E862. PMID: 27589778

In an area representative of a moderate climate zone (Lubuskie Province in Poland), mycological tests in over 270 flats demonstrated the occurrence of 82 species of moulds. Aspergillus versicolor Tiraboschi was often encountered on building partitions (frequency 4: frequently). The ability to synthesize the carcinogenic sterigmatocystin (ST) means that it poses a risk to humans and animals.

 

Mikkola R, Andersson MA, Hautaniemi M, Salkinoja-Salonen MS. Toxic indole alkaloids avrainvillamide and stephacidin B produced by a biocide tolerant indoor mold Aspergillus westerdijkiae. Toxicon. 2015 Jun 1;99:58-67. PMID: 25804991

Toxic Aspergillus westerdijkiae were present in house dust and indoor air fall-out from a residence and a kindergarten where the occupants suffered from building related ill health. The A. westerdijkiae isolates produced indole alkaloids avrainvillamide (445 Da) and its dimer stephacidin B (890 Da). It grew and sporulated in presence of high concentrations of boron or polyguanidine (PHMB, PHMG) based antimicrobial biocides used to remediate mold infested buildings.

 

McMullin DR, Nsiama TK, Miller JD. Secondary metabolites from Penicillium corylophilum isolated from damp buildings. Mycologia. 2014 Jul-Aug;106(4):621-8. PMID: 24891425

Penicillium corylophilum is surprisingly common in damp buildings in USA, Canada and western Europe. We examined isolates of P. corylophilum geographically distributed across Canada in the first comprehensive study of secondary metabolites of this fungus. The sesquiterpene phomenone, the meroterpenoids citreohybridonol and andrastin A, koninginin A, E and G, three new alpha pyrones and four new isochromans were identified from extracts of culture filtrates.

 

Täubel M, Sulyok M, Vishwanath V, Bloom E, Turunen M, Järvi K, Kauhanen E, Krska R, Hyvärinen A, Larsson L, Nevalainen A. Co-occurrence of toxic bacterial and fungal secondary metabolites in moisture-damaged indoor environments. Indoor Air. 2011 Oct;21(5):368-75. PMID: 21585551

In our study, we applied a multi-analyte tandem mass spectrometry-based methodology on sample materials of severely moisture-damaged homes, aiming to qualitatively and quantitatively describe the variety of microbial metabolites occurring in building materials and different dust sample types. For the first time, the presence of toxic bacterial metabolites and their co-occurrence with mycotoxins were shown for indoor samples. We show that toxic bacterial metabolites need to be considered as being part of very complex and diverse microbial exposures in ‘moldy’ buildings.

 

Andersen B, Frisvad JC, Søndergaard I, Rasmussen IS, Larsen LS. Associations between fungal species and water-damaged building materials. Appl Environ Microbiol. 2011 Jun;77(12):4180-8. PMID: 21531835

One aim of this study was to estimate the qualitative and quantitative diversity of fungi growing on damp or water-damaged building materials. Another was to determine if associations exist between the most commonly found fungal species and different types of materials. Analyses show that associated mycobiotas exist on different building materials.

 

Bloom E, Nyman E, Must A, Pehrson C, Larsson L. Molds and mycotoxins in indoor environments–a survey in water-damaged buildings.  Occup Environ Hyg. 2009 Nov;6(11):671-8. PMID: 19757292

We studied the prevalence of selected, potent mycotoxins and levels of fungal biomass in samples collected from water-damaged indoor environments in Sweden during a 1-year period. We show that (a) molds growing on a range of different materials indoors in water-damaged buildings generally produce mycotoxins, and (b) mycotoxin-containing particles in mold-contaminated environments may settle on surfaces above floor level.

 

Fogle MR, Douglas DR, Jumper CA, Straus DC. Growth and mycotoxin production by Chaetomium globosum is favored in a neutral pH. Int J Mol Sci. 2008 Dec;9(12):2357-65. PMID: 19330080

Chaetomium globosum is frequently isolated in water-damaged buildings and produces two mycotoxins called chaetoglobosins A and C when cultured on building material. In this study, the influence of ambient pH on the growth of C. globosum was examined on an artificial medium. This fungus was capable of growth on potato dextrose agar ranging in pH from 4.3 to 9.4 with optimal growth and chaetoglobosin C production occurring at a neutral pH. In addition, our results show that sporulation is favored in an acidic environment.

 

Gottschalk C, Bauer J, Meyer K. Detection of satratoxin g and h in indoor air from a water-damaged building. Mycopathologia. 2008 Aug;166(2):103-7. PMID: 18443920

The occurrence of Stachybotrys chartarum in indoor environments has been linked to adverse health effects as well as few cases of pulmonary haemorrhages in humans. Herein, a case of a LC-MS/MS-confirmed occurrence of airborne S. chartarum-toxins in a water-damaged dwelling is reported. Satratoxin G (0.25 ng/m(3)) and satratoxin H (0.43 ng/m(3)) were detected.

 

Seo SC, Reponen T, Levin L, Borchelt T, Grinshpun SA. Aerosolization of particulate (1–>3)-beta-D-glucan from moldy materials. Appl Environ Microbiol. 2008 Feb;74(3):585-93. PMID: 18065630

The purpose of this study was to characterize the release of particulate (1–>3)-beta-D-glucan from the surface of artificially mold-contaminated materials. Aspergillus versicolor and Stachybotrys chartarum were grown on malt extract agar (MEA), white ceiling tiles, and a wall-papered gypsum board for 1 and 6 months. These findings indicate that the use of malt extract agar in aerosolization experiments is likely to underestimate the release of S. chartarum particles from building materials.

 

Thacker PD. Airborne mycotoxins discovered in moldy buildings. Environ Sci Technol. 2004 Aug 1;38(15):282A. PMID: 15352435

 

Fog Nielsen K. Mycotoxin production by indoor molds. Fungal Genet Biol. 2003 Jul;39(2):103-17. PMID: 12781669

Fungal growth in buildings starts at a water activity (a(w)) near 0.8, but significant quantities of mycotoxins are not produced unless a(w) reaches 0.95. Stachybotrys generates particularly high quantities of many chemically distinct metabolites in water-damaged buildings. These metabolites are carried by spores, and can be detected in air samples at high spore concentrations. Very little attention has been paid to major metabolites of Stachybotrys called spirocyclic drimanes, and the precise structures of the most abundant of these compounds are unknown. Species of Aspergillus and Penicillium prevalent in the indoor environment produce relatively low concentrations of mycotoxins, with the exception of sterigmatocystins that can represent up to 1% of the biomass of A. versicolor at a(w)’s close to 1. The worst-case scenario for homeowners is produced by consecutive episodes of water damage that promote fungal growth and mycotoxin synthesis, followed by drier conditions that facilitate the liberation of spores and hyphal fragments.

 

Nieminen SM, Kärki R, Auriola S, Toivola M, Laatsch H, Laatikainen R, Hyvärinen A, Von Wright A. Isolation and identification of Aspergillus fumigatus mycotoxins on growth medium and some building materials. Appl Environ Microbiol. 2002 Oct;68(10):4871-5. PMID: 12324333

Genotoxic and cytotoxic compounds were isolated and purified from the culture medium of an indoor air mold, Aspergillus fumigatus. One of these compounds was identified as gliotoxin, a known fungal secondary metabolite. Growth of A. fumigatus and gliotoxin production on some building materials were also studied. Strong growth of the mold and the presence of gliotoxin were detected on spruce wood, gypsum board, and chipboard under saturation conditions.

 

Nielsen KF. Mycotoxins from mould infested building materials. Mycotoxin Res. 2000 Mar;16 Suppl 1:113-6. PMID: 23605430

Penicillium chrysogenum and A. ustus do not seem to produce any known mycotoxins when growing on building materials, whereasP. brevicompactum produces mycophenolic acid, someP. polonicum produces verrucosidin and verrucofortine,A. versicolor produces sterigmatocystins,A. niger produces nigragillin, orlandin, naphtho-γ-pyrones and tetracyclic compounds, some A. ochraceus produces ochratoxin A, Alternaria spp. produce alternariol and alternariol monomethyl ether, Chaetomium globosum produce chaetoglobosins, and finally 30-40% of Stachybotrys chartarum isolates from buildings produce macrocyclic trichothecenes and a number of other biologically active compounds.

 

Nielsen KF, Gravesen S, Nielsen PA, Andersen B, Thrane U, Frisvad JC. Production of mycotoxins on artificially and naturally infested building materials. Mycopathologia. 1999;145(1):43-56. PMID: 10560628

In this study, the ability to produce mycotoxins during growth on artificially infested building materials was investigated for Penicillium chrysogenum, Pen. polonicum, Pen. brevicompactum, Chaetomium spp., Aspergillus ustus, Asp. niger, Ulocladium spp., Alternaria spp., and Paecilomyces spp., all isolated from water-damaged building materials.

 

Gravesen S, Nielsen PA, Iversen R, Nielsen KF. Microfungal contamination of damp buildings–examples of risk constructions and risk materials. Environ Health Perspect. 1999 Jun;107 Suppl 3:505-8. PMID: 10347000

To elucidate problems with microfungal infestation in indoor environments, a multidisciplinary collaborative pilot study, supported by a grant from the Danish Ministry of Housing and Urban Affairs, was performed on 72 mold-infected building materials from 23 buildings.

 

Building Testing

Švajlenka J, Kozlovská M, Pošiváková T. Assessment and biomonitoring indoor environment of buildings. Int J Environ Health Res. 2017 Oct;27(5):427-439. PMID: 28868901

The case study presented here aims to demonstrate the effectiveness of the diagnostic methods used in assessing the presence of micromycetes in a building’s internal atmosphere and on the internal surfaces of a construction built using traditional construction methods. The methodology of comparing methods is based on their effectiveness, taking into account the identification of type and intensity of micromycetes presence in the air and on the material surfaces in the monitored areas.

 

Došen I, Andersen B, Phippen CB, Clausen G, Nielsen KF. Stachybotrys mycotoxins: from culture extracts to dust samples. Anal Bioanal Chem. 2016 Aug;408(20):5513-26. PMID: 27255106

Samples collected from walls contaminated by S. chartarum in a water-damaged building showed that the two known chemotypes, S and A, coexisted. More importantly, a link between mycotoxin concentrations found on contaminated surfaces and in settled dust was made. One dust sample, collected from a water-damaged room, contained 10 pg/cm(2) macrocyclic trichothecenes (roridin E). For the first time, more than one spirocyclic drimane was detected in dust. Spirocyclic drimanes were detected in all 11 analysed dust samples and in total amounted to 600 pg/cm(2) in the water-damaged room and 340 pg/cm(2) in rooms adjacent to the water-damaged area. Their wide distribution in detectable amounts in dust suggested they could be good candidates for exposure biomarkers.

 

Betancourt DA, Krebs K, Moore SA, Martin SM. Microbial volatile organic compound emissions from Stachybotrys chartarum growing on gypsum wallboard and ceiling tile. BMC Microbiol. 2013 Dec 5;13:283. PMID: 24308451

The aim of this study was to characterize MVOC emission profiles of seven toxigenic strains of S. chartarum, isolated from water-damaged buildings, in order to identify unique MVOCs generated during growth on gypsum wallboard and ceiling tile coupons. MVOCs are suitable markers for fungal identification because they easily diffuse through weak barriers like wallpaper, and could be used for early detection of mold growth in hidden cavities. This study identifies the production of anisole by seven toxigenic strains of Stachybotrys chartarum within a period of one week of growth on gypsum wallboard and ceiling tiles.

 

Cabral JP. Can we use indoor fungi as bioindicators of indoor air quality? Historical perspectives and open questions. Sci Total Environ. 2010 Sep 15;408(20):4285-95. PMID: 20655574

In sick houses and buildings, high indoor humidity allows fungal growth (mainly of Penicillium and Aspergillus), with concomitant release of conidia and fragments into the atmosphere. The intoxication probably results from a chronic exposure to volatile organic compounds and mycotoxins produced by Penicillium, Aspergillus, and Stachybotrys. It was concluded that fungi can be useful indicators of indoor air quality.

 

Bloom E, Bal K, Nyman E, Must A, Larsson L. Mass spectrometry-based strategy for direct detection and quantification of some mycotoxins produced by Stachybotrys and Aspergillus spp. in indoor environments. Appl Environ Microbiol. 2007 Jul;73(13):4211-7. PMID: 17483261

This is the first report on the use of tandem mass spectrometry for demonstrating mycotoxins in dust settled on surfaces above floor level in damp buildings. The direct detection of the highly toxic sterigmatocystin and macrocyclic trichothecene mycotoxins in indoor environments is important due to their potential health impacts.

 

Bloom E, Bal K, Nyman E, Larsson L. Optimizing a GC-MS method for screening of Stachybotrys mycotoxins in indoor environments. J Environ Monit. 2007 Feb;9(2):151-6. PMID: 17285157

Presence of Stachybotrys chartarum in indoor environments has been linked to building-associated disease, however, the causative agents are unknown. Verrucarol (VER) and trichodermol (TRID) are hydrolysis products of some major S. chartarum mycotoxins, i.e. macrocyclic trichothecenes and trichodermin. We optimized gas chromatography-mass spectrometry (GC-MS) methods for detecting VER and TRID in S. chartarum-contaminated indoor environmental samples. In summary, we have shown that NICI-GC-MSMS can be used to demonstrate mycotoxins in house dust in S. chartarum-contaminated dwellings.

 

Portnoy JM, Kennedy K, Barnes C. Sampling for indoor fungi: what the clinician needs to know. Curr Opin Otolaryngol Head Neck Surg. 2005 Jun;13(3):165-70. PMID: 15908815

Prevention of fungal contamination involves removal of moisture sources and humidity and early identification. If fungi are found on indoor surfaces, they can be removed using a dilute bleach/detergent solution that both kills the microorganisms and denatures allergens and toxins. Larger areas require professional remediation.

 

Portnoy JM, Barnes CS, Kennedy K. Sampling for indoor fungi. J Allergy Clin Immunol. 2004 Feb;113(2):189-98; quiz 199. PMID: 14767427

Fungi cause 3 primary adverse effects: (1) they can damage a building, (2) they can render a building unpleasant to live in by looking and smelling bad, and (3) they might cause adverse health effects in sensitive individuals. Sampling methods used to test hypotheses include air sampling for spores, measurement of allergens in house dust, and determination of microbially generated volatile organic compounds, ergosterols, glucans, and mycotoxins, as well as environmental conditions that lead to fungal contamination.

 

Tuomi T, Reijula K, Johnsson T, Hemminki K, Hintikka EL, Lindroos O, Kalso S, Koukila-Kähkölä P, Mussalo-Rauhamaa H, Haahtela T. Mycotoxins in crude building materials from water-damaged buildings. Appl Environ Microbiol. 2000 May;66(5):1899-904. PMID: 10788357

We analyzed 79 bulk samples of moldy interior finishes from Finnish buildings with moisture problems for 17 mycotoxins, as well as for fungi that could be isolated using one medium and one set of growth conditions. We found the aflatoxin precursor, sterigmatocystin, in 24% of the samples and trichothecenes in 19% of the samples. We conclude that the identification and enumeration of fungal species present in bulk materials are important to verify the severity of mold damage but that chemical analyses are necessary if the goal is to establish the presence of mycotoxins in moldy materials.

 

Building Remediation

Peitzsch M, Bloom E, Haase R, Must A, Larsson L. Remediation of mould damaged building materials–efficiency of a broad spectrum of treatments. J Environ Monit. 2012 Mar;14(3):908-15. PMID: 22286589

We compared the efficiency of some commercially available products and methods used for remediation of mould-contaminated building materials. Samples of gypsum board and pinewood were artificially contaminated with toxin-producing isolates of Stachybotrys chartarum and Aspergillus versicolor, respectively, then, ten different remediation treatments were applied according to the manufacturers’ instructions. None of the decontamination methods tested could completely eliminate viable moulds. Some methods, especially boron based chemicals, ammonium based chemicals, and oxidation reduced the contents of mycotoxins produced by S. chartarum (satratoxin G and H, verrucarol), whereas the one which uses an ammonium based chemical reduced the amount of sterigmatocystin produced by A. versicolor with statistical significance.

 

Lee TG. Mold remediation in a hospital. Toxicol Ind Health. 2009 Oct-Nov;25(9-10):723-30. PMID: 19854823

This paper is based on mold remediation of one portion of a hospital unit due to water from construction activity and inadequate maintenance, resulting in mold growth.

 

Wilson SC, Wu C, Andriychuk LA, Martin JM, Brasel TL, Jumper CA, Straus DC. Effect of chlorine dioxide gas on fungi and mycotoxins associated with sick building syndrome. Appl Environ Microbiol. 2005 Sep;71(9):5399-403. PMID: 16151130

The efficacy of chlorine dioxide gas as a fumigation treatment for inactivating sick building syndrome-related fungi and their mycotoxins was evaluated. These data show that chlorine dioxide gas can be effective to a degree as a fumigant for the inactivation of certain fungal colonies, that the perithecia of C. globosum can play a slightly protective role for the ascospores and that S. chartarum, while affected by the fumigation treatment, still remains toxic.

 

Hiipakka DW, Buffington JR. Resolution of sick building syndrome in a high-security facility. Appl Occup Environ Hyg. 2000 Aug;15(8):635-43. PMID: 10957819

The main objective of this article is to serve as a case study for other industrial hygiene (IH) professionals’ review as a “real world” effort in responding to a facility perceived as “sick” by its occupants. As many industrial hygienists do not have extensive backgrounds in evaluating microbial air contaminants or the mechanical function of building HVAC units, the overall intent is to provide “lessons learned” to IH generalists who may be asked to participate in indoor environmental quality (IEQ) surveys.