Skip to main content
Log in

Fungal secondary metabolites as harmful indoor air contaminants: 10 years on

  • Mini-Review
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

From the epidemiological studies conducted on the effect of mould and dampness on health a decade ago, the role of toxin-producing fungi in damp and mouldy buildings involved opinion more than evidence. Very little was known about the metabolites that were produced by the fungi that grew on damp building materials, and almost nothing had been reported on their occurrence in buildings. As a consequence, the focus was on speculations involving the fungal toxins that occur in agriculture. Over the past decade, particularly in the last 5 years, considerable progress has been made concerning the relevant toxins from fungi that grow on damp building materials. This paper summarizes the available data on the low-molecular-weight toxins reliably known from fungi common on damp building materials, the toxins that have been measured on mouldy building materials and the new understanding of the role that they play in the documented health effects of individuals living and working in damp and mouldy buildings.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Adan O, Huinink H, Bekker M (2011) Water relations of fungi in indoor environments. In: Fundamentals of mold growth in indoor environments and strategies for healthy living. Wageningen Academic Publishers, The Netherlands, pp 41–65

    Google Scholar 

  • AIHA (2008a) Mold ecology: recovery of fungi from certain moldy building materials. In: Prezant B, Weekes D, Miller JD (eds) Recognition, evaluation and control of indoor mold. American Industrial Hygiene Association, Fairfax, pp 43–51

    Google Scholar 

  • AIHA (2008b) Physical inspection of specific building types. In: Prezant B, Weekes D, Miller JD (eds) Recognition, evaluation and control of indoor mold. American Industrial Hygiene Association, Fairfax, pp 83–96

    Google Scholar 

  • Akpinar‐Elci M, White SK, Siegel PD, Park JH, Visotcky A, Kreiss K, Cox‐Ganser JM (2013) Markers of upper airway inflammation associated with microbial exposure and symptoms in occupants of a water‐damaged building. Am J Ind Med 56:522–530

    PubMed  Google Scholar 

  • Amend AS, Seifert KA, Bruns TD (2010) Quantifying microbial communities with 454 pyrosequencing: does read abundance count? Mol Ecol 19:5555–5565

    CAS  PubMed  Google Scholar 

  • Andersen B, Krøger E, Roberts RG (2001) Chemical and morphological segregation of Alternaria alternata, A. gaisen and A. longipes. Mycol Res 105:291–299

    CAS  Google Scholar 

  • Andersen B, Nielsen KF, Jarvis BB (2002) Characterization of Stachybotrys from water-damaged buildings based on morphology, growth and metabolite production. Mycologia 94:392–403

    CAS  PubMed  Google Scholar 

  • Andersen B, Nielsen KF, Thrane U, Cruse M, Taylor J, Jarvis BB (2003) Stachybotrys chlorohalonata, a new species from water damaged buildings. Mycologia 95:1228–1237

    Google Scholar 

  • Andersen B, Frisvad J, Søndergaard I, Rasmussen I, Larsen L (2011) Associations between fungal species and water-damaged building materials. J Appl Environ Microbiol 77:4180–4188

    CAS  Google Scholar 

  • Ayerst G (1969) The effects of moisture and temperature on growth and spore germination in some fungi. J Stored Prod Res 5:127–141

    Google Scholar 

  • Benítez T, Villa TG, Acha IG (1975) Chemical and structural differences in mycelial and regeneration walls of Trichoderma viride. Arch Microbiol 105:277–82

    PubMed  Google Scholar 

  • Biddle J (2008) Explaining the spread of residential air conditioning, 1955–1980. Explor Econ Hist 45:402–423

    Google Scholar 

  • Bloom E, Bal K, Nyman E, Must A, Larsson L (2007) Mass spectrometry based strategy for the direct detection and quantification of some mycotoxins produced by Stachybotrys and Aspergillus spp. in indoor environments. J Appl Environ Microbiol 73:4211–4217

    CAS  Google Scholar 

  • Bloom E, Nyman E, Must A, Pehrson C, Larsson L (2009) Mold and mycotoxins in indoor environments—a survey in water damaged buildings. J Occup Environ Hyg 6:671–678

    CAS  PubMed  Google Scholar 

  • Bomberg M (2013) Heat, air and moisture interactions. Front Archit Res 2:116–119

    Google Scholar 

  • Brown JS, Wilson WE, Grant LD (2005) Dosimetric comparisons of particle deposition and retention in rats and humans. Inhal Toxicol 17:355–385

    CAS  PubMed  Google Scholar 

  • Cairns-Fuller V, Aldred D, Magan N (2005) Water, temperature and gas composition interactions affect growth and ochratoxin A production by isolates of Penicillium verrucosum on wheat grain. J Appl Microbiol 99:1215–1221

    CAS  PubMed  Google Scholar 

  • Cho S, Seo S, Schmechel D, Grinshpun S, Reponen T (2005) Aerodynamic characteristics and respiratory deposition of fungal fragments. Atmos Environ 39:5454–5465

    CAS  Google Scholar 

  • Cox-Ganser JM, White SK, Jones R, Hilsbos K, Storey E, Enright PL, Rao CY, Kreiss K (2005) Respiratory morbidity in office workers in a water-damaged building. Environ Health Perspect 113:485–490

    PubMed Central  PubMed  Google Scholar 

  • Croft WA, Jarvis BB, Yatawara CS (1986) Airborne outbreak of trichothecene toxicosis. Atmos Environ 20:549–52

    Google Scholar 

  • Dales RE, Miller JD (1999) Residential fungal contamination and health: microbial cohabitants as covariates. Environ Health Perspect 107:481–483

    PubMed Central  PubMed  Google Scholar 

  • Dales R, Liu L, Wheeler AJ, Gilbert NL (2008) Quality of indoor residential air and health. CMAJ 179:147–152

    PubMed Central  PubMed  Google Scholar 

  • De Boer R (2000) Explaining house dust mite infestations on the basis of temperature and air humidity measurements. In: R. Siebers et al. (eds) Mites, asthma and domestic design III, Wellington, pp 13–19

  • De La Campa R, Seifert K, Miller JD (2007) Toxins from strains of Penicillium chrysogenum isolated from buildings and other sources. Mycopathologia 163:161–168

    CAS  PubMed  Google Scholar 

  • Desroches T, McMullin DR, Miller JD (2014) Extrolites of Wallemia sebi, a very common fungus in the built environment. Indoor Air 5:533–542

    Google Scholar 

  • Engelhart S, Loock A, Skutlarek D, Sagunski H, Lommel A, Farber H, Exner M (2002) Occurrence of toxigenic Aspergillus versicolor isolates and sterigmatocystin in carpet dust from damp indoor environments. Appl Environ Microbiol 68:3886–3890

    CAS  PubMed Central  PubMed  Google Scholar 

  • Flannigan B (1987) Mycotoxins in the air. Int Biodeterior 23:73–78

    CAS  Google Scholar 

  • Flannigan B, Miller JD (2011) Microbial growth in indoor environments. In: Flannigan B, Samson RA, Miller JD (eds) Microorganisms in home and indoor work environments: diversity, health impacts, investigation and control, 2nd edn. Taylor & Francis, New York, pp 57–107

    Google Scholar 

  • Fogle M, Douglas D, Jumper C, Straus DC (2007) Growth and mycotoxin production by Chaetomium globosum. Mycopathologia 164:49–56

    CAS  PubMed  Google Scholar 

  • Foto M, Plett J, Berghout J, Miller JD (2004) Modification of the Limulus amebocyte lysate assay for the analysis of glucan in indoor environments. Anal Bioanal Chem 379:156–162

    CAS  PubMed  Google Scholar 

  • Foto M, Vrijmoed LLP, Miller JD, Ruest K, Lawton M, Dales RE (2005) Comparison of airborne ergosterol, glucan and Air-O-Cell data in relation to physical assessments of mold damage and some other parameters. Indoor Air 15:256–266

    Google Scholar 

  • Frank M, Kingston E, Jeffery J, Moss M, Murray M, Simpson T, Sutherland A (1999) Walleminol and walleminone, novel caryophyllenes from the toxigenic fungus Wallemia sebi. Tetrahedron Lett 40:133–136

    CAS  Google Scholar 

  • Frazer S, Magan N, Aldred D (2011) The influence of water activity and temperature on germination, growth and sporulation of Stachybotrys chartarum strains. Mycopathologia 172:17–23

    PubMed  Google Scholar 

  • Frazer S, Pestka J, Kim J, Medina AD, Magan N (2012) Impact of environmental factors on growth and satratoxin G production by strains of Stachybotrys chartarum. World Mycotoxin J 5:37–43

    CAS  Google Scholar 

  • Frisvad JC, Thrane U (1995) Mycotoxin production by food-borne fungi. In: Samson RA, Hoekstra ES, Frisvad JC, Filtenborg O (eds) Introduction to food-borne fungi. Centraalbureau voor Schimmelcultures, Delft, pp 251–261

    Google Scholar 

  • Frisvad JC, Thrane U (2002) Mycotoxin production by common filamentous fungi. In: Samson RA, Hoekstra ES, Frisvad JC, Filtenborg O (eds) Introduction to food- and air borne fungi, 6th edn. Centraalbureau voor Schimmelcultures, Utrecht, pp 321–330

    Google Scholar 

  • Green BJ, Schmechel D, Summerbell R (2011) Aerosolized fungal fragments. In: Fundamentals of mold growth in indoor environments and strategies for healthy living. Wageningen Academic Publishers, The Netherlands, pp 211–243

    Google Scholar 

  • Gregory L, Pestka J, Dearborn D, Rand T (2004) Localization of satratoxin-G in Stachybotrys chartarum spores and spore-impacted mouse lung using immunocytochemistry. Toxicol Pathol 32:26–34

    CAS  PubMed  Google Scholar 

  • Gutarowska B, Sulyok M, Krska R (2010) A study of the toxicity of moulds isolated from dwellings. Indoor Built Environ 19:668–675

    Google Scholar 

  • Hay RJ (1995) Sick library syndrome. Lancet 346:1573–1574

    CAS  PubMed  Google Scholar 

  • Health Canada (2007) Residential indoor air quality guidelines: moulds. Health Canada, Ottawa

  • Hendry K, Cole E (1993) A review of mycotoxins in indoor air. J Toxicol Environ Health A 38:183–198

    CAS  Google Scholar 

  • Hinkley SF, Jiang J, Mazzola EP, Jarvis BB (1999) Atranones: novel diterpenoids from the toxigenic mold Stachybotrys atra. Tetrahedron Lett 40:2725–2728

    CAS  Google Scholar 

  • Hinkley SF, Mazzola EP, Fettinger JC, Lam YF, Jarvis BB (2000) Atranones A–G, from the toxigenic mold Stachybotrys chartarum. Phytochem 55:663–673

    CAS  Google Scholar 

  • Hite SC, Bray JL (1949) Research in home humidity control Research Series No. 106, Engineering Experiment Station. Purdue University, Lafayette

    Google Scholar 

  • Horner E, Miller JD (2003) Microbial volatile organic compounds with emphasis on those arising from filamentous fungal contaminants of buildings. ASHRAE Trans 109:215–231

    CAS  Google Scholar 

  • Houbraken J, Frisvad JC, Samson RA (2011) Fleming’s penicillin producing strain is not Penicillium chrysogenum but P. rubens. IMA Fungus 2:87–95

    PubMed Central  PubMed  Google Scholar 

  • IARC (2012) Improving public health through mycotoxin control. International Agency for Research on Cancer Scientific Publications Series, Lyon

  • Jaakkola M, Quansah R, Hugg T, Heikkinen S, Jaakkola J (2013) Association of indoor dampness and molds with rhinitis risk: a systematic review and meta-analysis. J Allergy Clin Immunol 132:1099–1110

    PubMed  Google Scholar 

  • Jarvis BB (2003) Analysis for mycotoxins: the chemist’s perspective. Arch Environ Health 58:479–483

    CAS  PubMed  Google Scholar 

  • Jarvis BB, Miller JD (2005) Mycotoxins as harmful indoor air contaminants. Appl Microbiol Biotechnol 66:367–372

    CAS  PubMed  Google Scholar 

  • Jarvis BB, Lee Y-W, Comezoglu N, Yatawara C (1986) Trichothecenes produced by Stachybotrys atra from Eastern Europe. Appl Environ Microbiol 51:915–918

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jarvis BB, Zhou Y, Jiang J, Wang S, Sorenson W, Hintikka E-L, Nikulin M, Parikka P, Etzel R, Dearborn D (1996) Toxigenic molds in water-damaged buildings: dechlorogriseofulvins from Memnoniella echinata. J Nat Prod 6:553–554

    Google Scholar 

  • Jarvis BB, Sorenson W, Hintikka E-L, Nikulin M, Zhou Y, Jiang J, Wang S, Hinkley S, Etzel R, Dearborn D (1998) Study of toxin production by isolates of Stachybotrys chartarum and Memnoniella echinata isolated during a study of pulmonary hemosiderosis in infants. Appl Environ Microbiol 64:3620–3625

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jedinak A, Dudhgaonkar S, Wu Q, Simon J, Sliva D (2011) Anti-inflammatory activity of edible oyster mushroom is mediated through the inhibition of NF-kB and AP-1 signaling. Nutr J 10:52

    CAS  PubMed Central  PubMed  Google Scholar 

  • Johnson L, Miller JD (2012) Consequences of large scale production of marijuana in residential buildings. Indoor Built Environ 21:595–600

    CAS  Google Scholar 

  • Korpi A, Pasanen A, Pasanen P, Kalliokoski P (1997) Microbial growth and metabolism in house dust. Int Biodeter Biodegradation 40:19–27

    Google Scholar 

  • Krieger J, Jacobs DE, Ashley PJ, Baeder A, Chew GL, Dearborn D, Hynes HP, Miller JD, Morley R, Rabito F, Zeldin DC (2010) Housing interventions and control of asthma-related indoor biologic agents: a review of the evidence. J Public Health Manag Pract 16:11–20

    Google Scholar 

  • Kurtböke DI (2012) Biodiscovery from rare actinomycetes: an eco-taxonomical perspective. Appl Microbiol Biotechnol 93:1843–1852

    PubMed  Google Scholar 

  • Levac SA (2011) Isolation, purification and characterization of proteins from indoor strains of Eurotium amstelodami, Eurotium rubrum and Eurotium herbariorum that are antigenic to humans. MSc Thesis, Carleton University

  • Li Y, Wadsö L (2013) Fungal activities of indoor moulds on wood as a function of relative humidity during desorption and adsorption processes. Eng Life Sci 13:528–535

    Google Scholar 

  • Liang Y, Zhao W, Xu J, Miller JD (2011) Characterization of two related exoantigens from the biodeteriogenic fungus Aspergillus versicolor. Int Biodeterior Biodegrad 65:217–226

    CAS  Google Scholar 

  • Lichtenstein J, Molina R, Donaghey T, Amuzie C, Pestka J, Coull B, Brain J (2010) Pulmonary responses to Stachybotrys chartarum and its toxins: mouse strain affects clearance and macrophage cytotoxicity. Toxicol Sci 116:113–121

    PubMed Central  PubMed  Google Scholar 

  • Lubeck M, Poulsen SK, Lubeck PS, Jensen DF, Thrane U (2000) Identification of Trichoderma strains from building materials by ITS1 ribotyping, UP-PCR fingerprinting and UP-PCR cross hybridization. FEMS Microbiol Lett 185:129–134

    CAS  PubMed  Google Scholar 

  • Maret R (1972) Chimie et morphologie submicroscopique des parois cellulaires de l’Ascomycète Chaetomium globosum. Arch Mikrobiol 81:68–90

    CAS  PubMed  Google Scholar 

  • McMullin DR (2014) Structural characterization of secondary metabolites produced by fungi obtained from damp Canadian buildings. PhD Dissertation, Carleton University

  • McMullin DR, Sumarah MW, Blackwell BA, Miller JD (2013a) New azaphilones from Chaetomium globosum isolated from the built environment. Tetrahedron Lett 54:568–572

    CAS  Google Scholar 

  • McMullin DR, Sumarah MW, Miller JD (2013b) Chaetoglobosins and azaphilones produced by Canadian strains of Chaetomium globosum isolated from the indoor environment. Mycotoxin Res 29:47–54

    CAS  PubMed  Google Scholar 

  • McMullin DR, Nsiama TK, Miller JD (2014a) Isochromans and α-pyrones from Penicillium corylophilum. J Nat Prod 77:206–212

    CAS  PubMed  Google Scholar 

  • McMullin DR, Nsiama TK, Miller JD (2014b) Secondary metabolites from Penicillium corylophilum isolated from damp buildings. Mycologia 106:621–628

    CAS  PubMed  Google Scholar 

  • Mendell MJ, Mirer AG, Cheung K, Tong M, Douwes J (2011) Respiratory and allergic health effects of dampness, mold, and dampness-related agents: a review of the epidemiologic evidence. Environ Health Perspect 119:748–756

    CAS  PubMed Central  PubMed  Google Scholar 

  • Mikkola R, Andersson M, Kredics L, Grigoriev P, Sundell N, Salkinoja-Salonen M (2012) 20-Residue and 11-residue peptaibols from the fungus Trichoderma longibrachiatum are synergistic in forming Na+/K+ -permeable channels and adverse action towards mammalian cells. FEBS J 279:4172–4190

    CAS  PubMed  Google Scholar 

  • Miller JD (1992) Fungi as contaminants of indoor air. Atmos Environ A 26:2163–2172

    Google Scholar 

  • Miller JD (1994a) Mycotoxins. In: Rylander R, Jacobs RR (eds) Handbook of organic dusts. Lewis Publishers, Boca Raton, pp 87–92

    Google Scholar 

  • Miller JD (1994b) Epidemiology of Fusarium graminearum diseases of wheat and corn. In: Miller JD, Trenholm HL (eds) Mycotoxins in grain: compounds other than aflatoxin. Eagan Press, St. Paul, pp 19–36

    Google Scholar 

  • Miller JD (2011) Health effects from mold and dampness in housing in western societies: early epidemiology studies and barriers to further progress. In: Adan O, Samson RA (eds) Molds, water, and the built environment. Wageningen Academic Press, The Netherlands, pp 229–245

    Google Scholar 

  • Miller JD, Richardson S (2013) Mycotoxins in Canada: a perspective for 2013. Regulatory Governance Initiative, pp 1–33

  • Miller JD, Young JC (1997) The use of ergosterol to measure exposure to fungal propagules. Am Ind Hyg Assoc J 58:39–43

    CAS  PubMed  Google Scholar 

  • Miller JD, Dugandzic R, Frescura A-M, Salares V (2007) Indoor and outdoor derived contaminants in urban and rural homes in Ottawa, Canada. J Air Waste Manag Assoc 57:297–302

  • Miller JD, Rand T, Jarvis BB (2003) Stachybotrys chartarum: cause of human disease or media darling? Med Mycol 41:271–291

    CAS  PubMed  Google Scholar 

  • Miller JD, Sun M, Gilyan A, Roy J, Rand TG (2010) Inflammation-associated gene transcription and expression in mouse lungs induced by low molecular weight compounds from fungi from the built environment. Chem Biol Interact 183:113–124

    CAS  PubMed  Google Scholar 

  • Miller JD, Schaafsma A, Bhatnagar D, Bondy G, Carbone I, Harris L, Harrison G, Munkvold G, Oswald I, Pestka J, Sharpe L, Sumarah M, Zhou T, Tittlemier S (2014) Mycotoxins that affect the North American agri-food sector: state of the art and directions for the future. World Mycotoxin J 7:63–82

    CAS  Google Scholar 

  • Murray DM, Burmaster DE (1995) Residential air exchange rates in the United States: empirical and estimated parametric distributions by season and climatic region. Risk Anal 15:459–465

    Google Scholar 

  • NAS (2000) Clearing the air: asthma and indoor air exposures. National Academy of Sciences. National Academy Press, Washington

    Google Scholar 

  • NAS (2004) Damp indoor spaces and health. Institute of Medicine National Academy of Sciences. National Academy Press, Washington

    Google Scholar 

  • Neveu WA, Bernardo E, Allard JL, Nagaleekar V, Wargo MJ, Davis RJ, Iwakura Y, Whittaker LA, Rincon M (2011) Fungal allergen β-glucans trigger p38 mitogen-activated protein kinase-mediated IL-6 translation in lung epithelial cells. Am J Respir Cell Mol Biol 45:1133–1141

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nielsen KF (2003) Mycotoxins production by indoor molds. Fungal Genet Biol 39:103–117

    CAS  Google Scholar 

  • Nielsen KF, Frisvad JC (2011) Mycotoxins in building materials. In: Fundamentals of mold growth in indoor environments and strategies for healthy living. Wageningen Academic Publishers, The Netherlands, pp 245–275

    Google Scholar 

  • Nielsen KF, Hansen M, Larsen T, Thrane U (1998a) Production of trichothecene mycotoxins on water damaged gypsum boards in Danish buildings. Int Biodeterior Biodegrad 42:1–7

    CAS  Google Scholar 

  • Nielsen KF, Thrane U, Larsen TO, Nielsen PA, Gravesen S (1998b) Production of mycotoxins on artificially inoculated building materials. Int Biodeterior Biodegrad 42:1–7

    CAS  Google Scholar 

  • Nielsen KF, Gravesen S, Nielsen P, Andersen B, Thrane U, Frisvad JC (1999) Production of mycotoxins on artificially and naturally infested building materials. Mycopathologia 145:43–56

    CAS  PubMed  Google Scholar 

  • Nielsen KF, Smedsgaard J, Larsen T, Lund F (2003) Chemical identification of fungi: metabolite profiling and metabolomics. Marcel Dekker, Inc, New York

    Google Scholar 

  • Nielsen KF, Holm G, Uttrup L, Nielsen P (2004) Mould growth on building materials under low water activities. Influence of humidity and temperature on fungal growth and secondary metabolism. Int Biodeterior Biodegrad 54:325–336

    CAS  Google Scholar 

  • Nielsen KF, Grafenhan T, Zafari D, Thrane U (2005) Trichothecene production by Trichoderma brevicompactum. J Agric Food Chem 53:8190–8196

    CAS  PubMed  Google Scholar 

  • Nielsen KF, Sumarah MW, Frisvad JC, Miller JD (2006) Production of metabolites by species in the Penicillium roqueforti complex. J Agric Food Chem 54:3756–3763

    CAS  PubMed  Google Scholar 

  • Nikulin M, Reijula K, Jarvis BB, Veijalainen P, Hintikka EL (1997) Effects of intranasal exposure to spores of Stachybotrys atra in mice. Fundam Appl Toxicol 35:182–188

    CAS  PubMed  Google Scholar 

  • NIOSH (2012) Preventing occupational respiratory disease from exposures caused by dampness in office buildings, schools, and other nonindustrial buildings. NIOSH Publication # 2013–102. Centers for Disease Control and Prevention, National Institute for Occupational Safety and Health. (www.cdc.gov/niosh)

  • Odabasi Z, Paetznick VL, Rodriguez JR, Chen E, McGinnis MR, Ostrosky-Zeichner L (2006) Differences in beta-glucan levels in culture supernatants of a variety of fungi. Med Mycol 44:267–272

    CAS  PubMed  Google Scholar 

  • Ohnishi T, Yamada G, Tanaka H, Nakajima K, Tanaka S, Morita-Ichimura S, Takahashi R, Sato M, Shibusa T, Abe S (2002) A case of chronic hypersensitivity pneumonia with elevation of serum SP-D and KL-6. Nihon Kokyuki Gakkai Zasshi 40:66–70

    PubMed  Google Scholar 

  • Pacheco-Sanchez M, Boutin Y, Angers P, Gosselin A, Tweddell RJ (2006) A bioactive (1 → 3)-, (1 → 4)-β-D glucan from Collybia dryophila and other mushrooms. Mycologia 98:180–185

    CAS  PubMed  Google Scholar 

  • Park JH, Cox-Ganser JM (2011) Mold exposure and respiratory health in damp indoor environments. Front Biosci 3:757–771

    Google Scholar 

  • Pasanen P, Pasanen A, Jantunen M (1993) Water condensation promotes fungal growth in ventilation ducts. Indoor Air 3:106–112

    Google Scholar 

  • Phalen RF, Oldham MJ, Wolf RK (2008) The relevance of animal models for aerosol studies. J Aerosol Med Pulm Drug Deliv 21:113–124

    PubMed  Google Scholar 

  • Provost NB, Shi C, She Y-M, Cyr TD, Miller JD (2013) Characterization of an antigenic chitosanase from the cellulolytic fungus Chaetomium globosum. Med Mycol 51:290–299

    CAS  PubMed  Google Scholar 

  • Quansah R, Jaakkola MS, Hugg T, Heikkinen SA, Jaakkola J (2012) Residential dampness and molds and the risk of developing asthma: a systematic review and meta-analysis. PLoS ONE 7:e47526

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rand TG, Miller JD (2008) Immunohistochemical and immunocytochemical detection of SchS34 antigen in Stachybotrys chartarum spores and spore impacted mouse lungs. Mycopathologia 165:73–80

    CAS  PubMed  Google Scholar 

  • Rand TG, Mahoney M, White K, Oulton M (2002) Microanatomical changes in alveolar type II cells in juvenile mice intratracheally exposed to Stachybotrys chartarum spores and toxin. Toxicol Sci 65:239–245

    CAS  PubMed  Google Scholar 

  • Rand TG, Flemming J, Giles S, Miller JD, Puniani E (2005) Inflammatory and cytotoxic responses in mouse lungs exposed to purified toxins from building isolates of Penicillium brevicompactum Dierckx and P. chrysogenum Thom. Toxicol Sci 87:213–222

    CAS  PubMed  Google Scholar 

  • Rand TG, Flemming J, Miller JD, Womiloju TO (2006) Comparison of inflammatory and cytotoxic responses in mouse lungs exposed to atranone A and C from Stachybotrys chartarum. Toxicol Environ Health 69:1239–1251

    CAS  Google Scholar 

  • Rand TG, Sun M, Gilyan A, Downey J, Miller JD (2010) Dectin-1 and inflammation-associated gene transcription and expression in mouse lungs by a toxic (1,3)-beta-D glucan. Arch Toxicol 84:205–220

    CAS  PubMed  Google Scholar 

  • Rand TG, DiPenta J, Robbins C, Miller JD (2011) Effects of low molecular weight fungal compounds on inflammatory gene transcription and expression in mouse alveolar macrophages. Chem Biol Interact 190:139–147

    CAS  PubMed  Google Scholar 

  • Rand TG, Robbins C, Rajaraman D, Sun M, Miller JD (2013) Induction of Dectin-1 and asthma- associated signal transduction pathways in RAW 264.7 cells by a triple helical (1, 3)-β-D glucan, curdlan. Arch Toxicol 87:1841–1850

    CAS  PubMed  Google Scholar 

  • Rao CY, Burge HA, Chang JC (1996) Review of quantitative standards and guidelines for fungi in indoor air. J Air Waste Manag Assoc 46:899–908

    CAS  PubMed  Google Scholar 

  • Rao CY, Fink RC, Wolfe LB, Liberman DF, Burge HA (1997) A study of aflatoxin production by Aspergillus flavus growing on wallboard. J Am Biol Saf Assoc 2:36–42

    Google Scholar 

  • Reino J, Guerro R, Hernandez R, Collado I (2008) Secondary metabolites from species of the biocontrol agent Trichoderma. Phytochem Rev 7:89–123

    CAS  Google Scholar 

  • Ren P, Ahearn DG, Crow SA (1998) Mycotoxins of Alternaria alternata produced on ceiling tiles. J Ind Microbiol 20:53–54

    CAS  Google Scholar 

  • Ren P, Ahearn DG, Crow SA (1999) Comparative study of Aspergillus mycotoxin production on enriched media and construction material. J Ind Microbiol Biotechnol 23:209–213

    CAS  Google Scholar 

  • Reponen T, Seo S, Grimsley F, Lee T, Crawford C, Grinshpun S (2007) Fungal fragments in moldy houses: a field study in homes in New Orleans and Southern Ohio. Atmos Environ 41:8140–8149

    CAS  PubMed Central  Google Scholar 

  • Richard J, Plattner R, Mary J, Liska S (1999) The occurrence of ochratoxin A in dust collected from a problem household. Mycopathologia 146:99–103

    CAS  PubMed  Google Scholar 

  • Richards R, Burch D, Thomas W (1992) Water vapor sorption measurements of common building materials. ASHRAE Trans 98:475p

    Google Scholar 

  • Salares VR, Hinde CA, Miller JD (2009) Analysis of settled dust in homes and fungal glucan in air particulate collected during HEPA vacuuming. Indoor Built Environ 18:485–491

    CAS  Google Scholar 

  • Salazar RR (1997) Production of ochratoxin A by Aspergillus ochraceus growing on ceiling tile and carpet. PhD dissertation, University of South Florida

  • Samson RA (1985) Occurrence of moulds in modern living and working environments. Eur J Epidemiol 1:54–61

    CAS  PubMed  Google Scholar 

  • Samson RA, Houbraken J, Thrane U, Frisvad JC, Andersen B (2010) Food and indoor fungi. CBS-KNAW Fungal Biodiversity Centre, Utrecht, p 390

    Google Scholar 

  • Samson RA, Visagie CM, Houbraken J, Hong S-B, Hubka V, Klaassen CHW, Perrone G, Seifert KA, Susca A, Tanney JB, Varga J, Kocsubé S, Szigeti G, Yaguchi Y, Frisvad JC (2014) Phylogeny, identification and nomenclature of the genus Aspergillus. Stud Mycol 78:141–178

    Google Scholar 

  • Schleibinger H, Laussmann D, Brattig C, Mangler M, Eis D, Ruden H (2005) Emission patterns and emission rates of MVOC and the possibility for predicting hidden mold damage? Indoor Air 15(s9):98–104

    PubMed  Google Scholar 

  • Scott PM (2009) Ergot alkaloids: extent of human and animal exposure. World Mycotoxin J 2:141–149

    CAS  Google Scholar 

  • Scott J, Untereiner WA, Wong B, Strauss NA, Malloch D (2004) Genotypic variation in Penicillium chrysogenum from indoor environments. Mycologia 96:1095–1105

    CAS  PubMed  Google Scholar 

  • Seifert KA, Frisvad JC (2000) Penicillium on solid wood products. In: Samson RA, Pitt JI (eds) Integration of modern taxonomic methods for Penicillium and Aspergillus classification. Harwood Academic Publishers, Amsterdam, pp 285–292

    Google Scholar 

  • Semeiks J, Borek D, Otwinowski Z, Grishin NV (2014) Comparative genome sequencing reveals chemotype-specific gene clusters in the toxigenic black mold Stachybotrys. BMC Genomics 15:590

    PubMed Central  PubMed  Google Scholar 

  • Slack GJ, Puniani E, Frisvad JC, Samson RA, Miller JD (2009) Secondary metabolites from Eurotium species, A. calidoustus and A. insuetus common in Canadian homes with a review of their chemistry and biological activities. Mycol Res 113:480–490

    CAS  PubMed  Google Scholar 

  • Smoragiewicz W, Cossette B, Boutard A, Krzystyniak K (1993) Trichothecene mycotoxins in the dust of ventilation systems in office buildings. Int Arch Occup Environ Health 65:113–117

    CAS  PubMed  Google Scholar 

  • Sonjak S, Frisvad JC, Gunde‐Cimerman N (2005) Comparison of secondary metabolite production by Penicillium crustosum strains, isolated from Arctic and other various ecological niches. FEMS Microbiol Ecol 53:51–60

    CAS  PubMed  Google Scholar 

  • Sorensen WG (1999) Fungal spores: hazardous to health? Environ Health Perspect 107(Suppl 3):469–472

    Google Scholar 

  • Sorenson WG (1989) Health impact of mycotoxins in the home and workplace: an overview. Biodeterior Res 2:201–215

    Google Scholar 

  • Sorenson WG (1990) Mycotoxins as potential occupational hazards. Dev Ind Micro 31:205–211

    CAS  Google Scholar 

  • Sorenson WG, Frazer DG, Jarvis BB, Simpson J, Robinson V (1987) Trichothecene mycotoxins in aerosolized conidia of Stachybotrys atra. Appl Environ Microbiol 53:1370–1375

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sumarah MW, Miller JD, Blackwell BA (2005) Isolation and metabolite production by Penicillium roqueforti, P. paneum and P. crustosum isolated in Canada. Mycopathol 159:571–577

    CAS  Google Scholar 

  • Täubel M, Sulyok M, Vishwanath V, Bloom E, Turunen M, Järvi K, Kauhanen E, Krska R, Hyvärinen A, Larsson L, Nevalainen A (2011) Co-occurrence of toxic bacterial and fungal secondary metabolites in moisture-damaged indoor environments. Indoor Air 21:368–375

    PubMed  Google Scholar 

  • TenWolde A and Pilon C (2007) The effect of indoor humidity on water vapor release in homes. In: ASHRAE proceedings of thermal performance of the exterior envelopes of whole buildings X International Conference, Clearwater, FL

  • Tobin RS, Baranowski E, Gilman AP, Kuiper-Goodman T, Miller JD, Giddings M (1987) Significance of fungi in indoor air: report of a working group. Can J Public Health 78:S1–32

    Google Scholar 

  • Visagie C, Hirooka Y, Tanney J, Whitfield E, Mwange K, Meijer M, Amend A, Seifert KA, Samson RA (2014) Aspergillus, Penicillium and Talaromyces isolated from house dust samples collected around the world. Stud Mycol 78:63–139

    Google Scholar 

  • Vishwanath V, Sulyok M, Labuda R, Bicker W, Krska R (2009) Simultaneous determination of 186 fungal and bacterial metabolites in indoor matrices by liquid chromatography tandem mass spectrometry. Anal Bioanal Chem 395:1355–1372

    CAS  PubMed  Google Scholar 

  • WHO (2009) Guidelines for indoor air quality: dampness and mould. World Health Organization. Regional Office for Europe, DK 2100, Copenhagen, Denmark

  • Williams DL (1997) Overview of 1,3-β-D-glucan immunobiology. Mediat Inflamm 6:247–250

    CAS  Google Scholar 

  • Williams DL, Lowman DW, Ensley HE (2005) Introduction to the chemistry and immunobiology of β-glucans. In: Young S-H, Castranova V (eds) Toxicology of 1–3 beta-glucans. CRC Press, Boca Raton, pp 1–34

    Google Scholar 

  • Wilson AW, Luo W, Miller JD (2009) Using human sera to identify a 52 kDa exoantigen of Penicllium chrysogenum and implications of polyphasic taxonomy of anamorphic ascomycetes in the study of allergens. Mycopathologia 168:213–226

    CAS  PubMed  Google Scholar 

  • Wood G, Mann P, Reid W, Moss M (1990) Studies on a toxic metabolite from the mould Wallemia. Food Addit Contam 7:69–77

    CAS  PubMed  Google Scholar 

  • Xu J, Jensen JT, Liang Y, Belisle D, Miller JD (2007) The biology and immogenicity of a 34 kDa antigen of Stachybotrys chartarum sensu lato. Int Biodeterior Biodegrad 60:308–318

    CAS  Google Scholar 

Download references

Acknowledgments

The preparation of this paper was funded by an NSERC IRC to JDM and an Ontario Graduate Scholarship (OGS) to DRM. Much is owed to Prof. Thomas Rand, St. Mary’s University, for his valued cooperation and scientific expertise over the past 15 years. The influence of Dr. Brian Flannigan, Edinburgh, and Prof. Dr. Rob Samson, CBS, The Netherlands, over many years on the thinking of J. David Miller is noted with appreciation. The majority of the strains discussed in this paper are deposited in recognized culture collections.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to J. David Miller.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Miller, J.D., McMullin, D.R. Fungal secondary metabolites as harmful indoor air contaminants: 10 years on. Appl Microbiol Biotechnol 98, 9953–9966 (2014). https://doi.org/10.1007/s00253-014-6178-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-014-6178-5

Keywords

Navigation