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Microbial Secondary Metabolites and Knowledge on Inhalation Effects

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Book cover Exposure to Microbiological Agents in Indoor and Occupational Environments

Abstract

Microbial secondary metabolites include compounds produced during the growth of both fungi and bacteria. These compounds are present in workplaces and indoor environments, although the concentrations of single toxins in the air are typically low. Inhalation is considered to be the most significant route of exposure for microbial secondary metabolites in indoor environments although exposure to microbial toxins may happen also via alimentary or dermal route. Inhalation effects of microbial secondary metabolites have been studied experimentally in vivo in animal models, mainly in rodents. In vitro studies with cells of respiratory system and ex vivo cultured tissues have elucidated the mechanisms of action for the most common toxins. However, there are only few epidemiological studies on health effects of mycotoxin exposure, and often the studies are limited by exposure assessment based on single compounds or surrogates of mycotoxin exposure. We summarize here studies on the inhalation effects of microbial toxins showing a wide variety of adverse health effects which are not limited to the respiratory system, and identify the knowledge gaps where future research efforts should be targeted.

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References

  • Amuzie CJ, Harkema JR, Pestka JJ (2008) Tissue distribution and proinflammatory cytokine induction by the trichothecene deoxynivalenol in the mouse: comparison of nasal vs. oral exposure. Toxicology 248:39–44. doi:10.1016/j.tox.2008.03.005

    Article  CAS  PubMed  Google Scholar 

  • Amuzie CJ, Islam Z, Kim JK et al. (2010) Kinetics of satratoxin G tissue distribution and excretion following intranasal exposure in the mouse. Toxicol Sci 116:433–440. doi:10.1093/toxsci/kfq142

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Autrup JL, Schmidt J, Seremet T et al. (1991) Determination of exposure to aflatoxins among Danish workers in animal-feed production through the analysis of aflatoxin B1 adducts to serum albumin. Scand J Work Environ Health 17:436–440

    Article  CAS  PubMed  Google Scholar 

  • Behm C, Föllmann W, Degen GH (2012) Cytotoxic potency of mycotoxins in cultures of V79 lung fibroblast cells. J Toxicol Environ Health A 75:1226–1231. doi:10.1080/15287394.2012.709170

    Article  CAS  PubMed  Google Scholar 

  • Bitnun A, Nosal RM (1999) Stachybotrys chartarum (atra) contamination of the indoor environment: health implications. Paediatr Child Health 4:125–129

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bloom E, Nyman E, Must A et al. (2009) Molds and mycotoxins in indoor environments – a survey in water-damaged buildings. J Occup Environ Hyg 6:671–678. doi:10.1080/15459620903252053

    Article  CAS  PubMed  Google Scholar 

  • Boonen J, Malysheva SV, Taevernier L et al. (2012) Human skin penetration of selected model mycotoxins. Toxicology 301:21–32. doi:10.1016/j.tox.2012.06.012

    Article  CAS  PubMed  Google Scholar 

  • Brasel TL, Campbell AW, Demers RE et al. (2004) Detection of trichothecene mycotoxins in sera from individuals exposed to Stachybotrys chartarum in indoor environments. Arch Environ Health 59:317–323

    CAS  PubMed  Google Scholar 

  • Brasel TL, Martin JM, Carriker CG et al. (2005) Detection of airborne Stachybotrys chartarum macrocyclic trichothecene mycotoxins in the indoor environment. Appl Environ Microbiol 71:7376–7388

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brewer JH, Thrasher JD, Hooper D (2013a) Chronic illness associated with mold and mycotoxins: is naso-sinus fungal biofilm the culprit? Toxins (Basel) 6:66–80. doi:10.3390/toxins6010066

    Article  CAS  Google Scholar 

  • Brewer JH, Thrasher JD, Straus DC et al. (2013b) Detection of mycotoxins in patients with chronic fatigue syndrome. Toxins (Basel) 5:605–617. doi:10.3390/toxins5040605

    Article  CAS  Google Scholar 

  • Burg WA, Shotwell OL, Saltzman BE (1981) Measurements of airborne aflatoxins during the handling of contaminated corn. Am Ind Hyg Assoc J 42:1–11. doi:10.1080/15298668191419271

    Article  CAS  PubMed  Google Scholar 

  • Burg WR, Shotwell OL, Saltzman BE (1982) Measurement of airborne aflatoxins during the handling of 1979 contaminated corn. Am Ind Hyg Assoc J 43:580–586

    Article  CAS  Google Scholar 

  • Cabaret O, Puel O, Botterel F et al. (2010) Metabolic detoxication pathways for sterigmatocystin in primary tracheal epithelial cells. Chem Res Toxicol 23:1673–1681. doi:10.1021/tx100127b

    Article  CAS  PubMed  Google Scholar 

  • Cai GH, Malarstig B, Kumlin A et al. (2011) Fungal DNA and plergen levels in Swedish day care centers and associations with building characteristics. J Environ Monit 13:2018–2024. doi:10.1039/c0em00553c

    Article  CAS  PubMed  Google Scholar 

  • Capasso L, Longhin E, Caloni F et al. (2015) Synergistic inflammatory effect of PM10 with mycotoxin deoxynivalenol on human lung epithelial cells. Toxicon 104:65–72. doi:10.1016/j.toxicon.2015.08.008

    Article  CAS  PubMed  Google Scholar 

  • Carey SA, Plopper CG, Hyde DM et al. (2012) Satratoxin-G from the black mold Stachybotrys chartarum induces rhinitis and apoptosis of olfactory sensory neurons in the nasal airways of rhesus monkeys. Toxicol Pathol 40:887–898. doi:10.1177/0192623312444028

    Article  PubMed  Google Scholar 

  • Chatopadhyay P, Tariang B, Agnihotri A et al. (2014) Synergism of ochratoxin B and calcium-channel antagonist verapamil caused mitochondrial dysfunction. Toxicol Mech Methods 24:428–432. doi:10.3109/15376516.2014.936543

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Corcuera LA, Vettorazzi A, Arbillaga L et al. (2015) Genotoxicity of aflatoxin B1 and ochratoxin A after simultaneous application of the in vivo micronucleus and comet assay. Food Chem Toxicol 76:116–124. doi:10.1016/j.fct.2014.12.003

    Article  CAS  PubMed  Google Scholar 

  • Corps KN, Islam Z, Pestka JJ et al. (2010) Neurotoxic, inflammatory, and mucosecretory responses in the nasal airways of mice repeatedly exposed to the macrocyclic trichothecene mycotoxin roridin A: dose-response and persistence of injury. Toxicol Pathol 38:429–451. doi:10.1177/0192623310364026

    Article  CAS  PubMed  Google Scholar 

  • Council for Agricultural Science and Technology (2003) Mycotoxins: risk in plant, animal, and human systems. Task force report 139, Ames, Iowa

    Google Scholar 

  • Creasia DA, Thurman JD, Jones 3rd LJ et al. (1987) Acute inhalation toxicity of T-2 mycotoxin in mice. Fundam Appl Toxicol 8:230–235

    Article  CAS  PubMed  Google Scholar 

  • Creasia DA, Thurman JD, Wannemacher Jr RW et al. (1990) Acute inhalation toxicity of T-2 mycotoxin in the rat and guinea pig. Fundam Appl Toxicol 14:54–59

    Article  CAS  PubMed  Google Scholar 

  • Croft WA, Jarvis BB, Yatatwara CS (1986) Airborne outbreak of trichothecene toxicosis. Atmos Environ 20:549–552

    Article  Google Scholar 

  • Croft WA, Jastromski BM, Croft AL et al. (2002) Clinical confirmation of trichothecene mycotoxicosis in patient urine. J Environ Biol 23:301–320

    PubMed  Google Scholar 

  • Degen G (2011) Tools for investigating workplace-related risks from mycotoxin exposure. World Mycotoxin J 4:315–327

    Article  Google Scholar 

  • Degen GH, Mayer S, Blaszkewicz M (2007) Biomonitoring of ochratoxin A in grain workers. Mycotoxin Res 23:88–93. doi:10.1007/BF02946032

    Article  CAS  PubMed  Google Scholar 

  • Dennis D, Robertson D, Curtis L et al. (2009) Fungal exposure endocrinopathy in sinusitis with growth hormone deficiency: Dennis-Robertson syndrome. Toxicol Ind Health 25:669–680. doi:10.1177/0748233709348266

    Article  CAS  PubMed  Google Scholar 

  • Di Paolo N, Guarnieri A, Garosi G et al. (1994) Inhaled mycotoxins lead to acute renal failure. Nephrol Dial Transplant 9(Suppl 4):116–120

    PubMed  Google Scholar 

  • Drew R, Frangos J (2007) The concentration of no toxicological concern (CoNTC): a risk assessment screening tool for air toxics. J Toxicol Environ Health A 70:1584–1593. 781628584 [pii]

    Article  CAS  PubMed  Google Scholar 

  • Driscoll KE, Costa DL, Hatch G et al. (2000) Intratracheal instillation as an exposure technique for the evaluation of respiratory tract toxicity: uses and limitations. Toxicol Sci 55:24–35

    Article  CAS  PubMed  Google Scholar 

  • Dvorácková I, Pichová V (1986) Pulmonary interstitial fibrosis with evidence of aflatoxin B1 in lung tissue. J Toxicol Environ Health 18:153–157. doi:10.1080/15287398609530856

    Article  PubMed  Google Scholar 

  • EU (2003) EU Directive 76/768/EEC, Directive 2003/15/EC of the European Parliament and of the Council. Off J Eur Union L66:26–35

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Föllmann W, Ali N, Blaszkewicz M et al. (2016) Biomonitoring of mycotoxins in urine: pilot study in mill workers. J Toxicol Environ Health A 79:1015–1025

    Article  PubMed  CAS  Google Scholar 

  • Forgacs J (1962) Mycotoxicoses – the neglected disease. Feedstuffs 34:124–134

    Google Scholar 

  • Fromme H, Gareis M, Völkel W et al. (2016) Overall internal exposure to mycotoxins and their occurrence in occupational and residential settings – an overview. Int J Hyg Environ Health 219:143–165. doi:10.1016/j.ijheh.2015.11.004

    Article  CAS  PubMed  Google Scholar 

  • González-Arias CA, Crespo-Sempere A, Marin S et al. (2015) Modulation of the xenobiotic transformation system and inflammatory response by ochratoxin A exposure using a co-culture system of Caco-2 and HepG2 cells. Food Chem Toxicol 86:245–252. doi:10.1016/j.fct.2015.10.007

    Article  PubMed  CAS  Google Scholar 

  • Gottschalk C, Bauer J, Meyer K (2008) Detection of satratoxin g and h in indoor air from a water-damaged building. Mycopathologia 166:103–107. doi:10.1007/s11046-008-9126-z

    Article  CAS  PubMed  Google Scholar 

  • Gruber-Dorninger C, Novak B, Nagl V, et al. (2016) Emerging mycotoxins: beyond traditionally determined food contaminants. J Agric Food Chem. doi:10.1021/acs.jafc.6b03413

  • Guindon-Kezis KA, Mulder JE, Massey TE (2014) In vivo treatment with aflatoxin B1 increases DNA oxidation, base excision repair activity and 8-oxoguanine DNA glycosylase 1 levels in mouse lung. Toxicology 321:21–26. doi:10.1016/j.tox.2014.03.004

    Article  CAS  PubMed  Google Scholar 

  • Hardin BD, Kelman BJ, Saxon A (2003) Adverse human health effects associated with molds in the indoor environment. J Occup Environ Med 45:470–478

    Article  PubMed  Google Scholar 

  • Hardin BD, Robbins CA, Fallah P et al. (2009) The concentration of no toxicologic concern (CoNTC) and airborne mycotoxins. J Toxicol Environ Health A 72:585–598. doi:10.1080/15287390802706389

    Article  CAS  PubMed  Google Scholar 

  • Harkema JR, Carey SA, Wagner JG (2006) The nose revisited: a brief review of the comparative structure, function, and toxicologic pathology of the nasal epithelium. Toxicol Pathol 34:252–269. H1080432VQ59X328 [pii]

    Article  CAS  PubMed  Google Scholar 

  • Hasegawa-Baba Y, Kubota H, Takata A et al. (2014) Intratracheal instillation methods and the distribution of administered material in the lung of the rat. J Toxicol Pathol 27:197–204. doi:10.1293/tox.2014-0022

    Article  PubMed  PubMed Central  Google Scholar 

  • Hayes RB, van Nieuwenhuize JP, Raatgever JW et al. (1984) Aflatoxin exposures in the industrial setting: an epidemiological study of mortality. Food Chem Toxicol 22:39–43

    Article  CAS  PubMed  Google Scholar 

  • Hodgson MJ, Morey P, Leung WY et al. (1998) Building-associated pulmonary disease from exposure to Stachybotrys chartarum and Aspergillus versicolor. J Occup Environ Med 40:241–249

    Article  CAS  PubMed  Google Scholar 

  • Hooper DG, Bolton VE, Guilford FT et al. (2009) Mycotoxin detection in human samples from patients exposed to environmental molds. Int J Mol Sci 10:1465–1475. doi:10.3390/ijms10041465

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hope JH, Hope BE (2012) A review of the diagnosis and treatment of ochratoxin A inhalational exposure associated with human illness and kidney disease including focal segmental glomerulosclerosis. J Environ Public Health 2012:835059. doi:10.1155/2012/835059

    Article  PubMed  CAS  Google Scholar 

  • Huttunen K, Pelkonen J, Nielsen KF et al. (2004) Synergistic interaction in simultaneous exposure to Streptomyces californicus and Stachybotrys chartarum. Environ Health Perspect 112:659–665

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iavicoli I, Brera C, Carelli G et al. (2002) External and internal dose in subjects occupationally exposed to ochratoxin A. Int Arch Occup Environ Health 75:381–386. doi:10.1007/s00420-002-0319-3

    Article  CAS  PubMed  Google Scholar 

  • Islam Z, Amuzie CJ, Harkema JR et al. (2007) Neurotoxicity and inflammation in the nasal airways of mice exposed to the macrocyclic trichothecene mycotoxin roridin a: kinetics and potentiation by bacterial lipopolysaccharide coexposure. Toxicol Sci 98:526–541.

    Article  CAS  PubMed  Google Scholar 

  • Islam Z, Harkema JR, Pestka JJ (2006) Satratoxin G from the black mold Stachybotrys chartarum evokes olfactory sensory neuron loss and inflammation in the murine nose and brain. Environ Health Perspect 114:1099–1107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Islam Z, Pestka JJ (2006) LPS priming potentiates and prolongs proinflammatory cytokine response to the trichothecene deoxynivalenol in the mouse. Toxicol Appl Pharmacol 211:53–63. S0041-008X(05)00223-1 [pii]

    Article  CAS  PubMed  Google Scholar 

  • Jakab GJ, Hmieleski RR, Zarba A et al. (1994) Respiratory aflatoxicosis: suppression of pulmonary and systemic host defenses in rats and mice. Toxicol Appl Pharmacol 125:198–205. S0041-008X(84)71065-9 [pii]

    Article  CAS  PubMed  Google Scholar 

  • Jarvis BB, Miller JD (2005) Mycotoxins as harmful indoor air contaminants. Appl Microbiol Biotechnol 66:367–372. doi:10.1007/s00253-004-1753-9

    Article  CAS  PubMed  Google Scholar 

  • Jia C, Sangsiri S, Belock B et al. (2011) ATP mediates neuroprotective and neuroproliferative effects in mouse olfactory epithelium following exposure to satratoxin G in vitro and in vivo. Toxicol Sci 124:169–178. doi:10.1093/toxsci/kfr213

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kankkunen P, Rintahaka J, Aalto A et al. (2009) Trichothecene mycotoxins activate inflammatory response in human macrophages. J Immunol 182:6418–6425. doi:10.4049/jimmunol.0803309

    Article  CAS  PubMed  Google Scholar 

  • Kankkunen P, Välimäki E, Rintahaka J et al. (2014) Trichothecene mycotoxins activate NLRP3 inflammasome through a P2X7 receptor and Src tyrosine kinase dependent pathway. Hum Immunol 75:134–140. doi:10.1016/j.humimm.2013.11.010

    Article  CAS  PubMed  Google Scholar 

  • Kelman BJ, Robbins CA, Swenson LJ et al. (2004) Risk from inhaled mycotoxins in indoor office and residential environments. Int J Toxicol 23:3–10. doi:10.1080/10915810490265423

    Article  CAS  PubMed  Google Scholar 

  • Kilburn KH (2009) Neurobehavioral and pulmonary impairment in 105 adults with indoor exposure to molds compared to 100 exposed to chemicals. Toxicol Ind Health 25:681–92. doi:10.1177/0748233709348390

    Article  PubMed  Google Scholar 

  • Kilburn KH, Thrasher JD, Immers NB (2009) Do terbutaline- and mold-associated impairments of the brain and lung relate to autism? Toxicol Ind Health 25:703–10. doi:10.1177/0748233709348391

    Article  CAS  PubMed  Google Scholar 

  • Kirjavainen PV, Täubel M, Karvonen AM et al. (2015) Microbial secondary metabolites in homes in association with moisture damage and asthma. Indoor Air 3:448–456. doi:10.1111/ina.12213

    Google Scholar 

  • Korkalainen M, Täubel M, Naarala J et al. (2017) Synergistic proinflammatory interactions of microbial toxins and structural components characteristic to moisture-damaged buildings. Indoor Air 27:13–23. doi:10.1111/ina.12282

    Article  CAS  PubMed  Google Scholar 

  • Korpi A, Järnberg J, Pasanen AL (2009) Microbial volatile organic compounds. Crit Rev Toxicol 39:139–93. doi:10.1080/10408440802291497

    Article  CAS  PubMed  Google Scholar 

  • KÅ‘szegi T, Poór M (2016) Ochratoxin A: molecular interactions, mechanisms of toxicity and prevention at the molecular level. Toxins 8:111. doi:10.3390/toxins8040111

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lai H, Mo X, Yang Y et al. (2014) Association between aflatoxin B1 occupational airway exposure and risk of hepatocellular carcinoma: a case-control study. Tumour Biol 35:9577–9584. doi:10.1007/s13277-014-2231-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Larsson P, Tjälve H (2000) Intranasal instillation of aflatoxin B(1) in rats: bioactivation in the nasal mucosa and neuronal transport to the olfactory bulb. Toxicol Sci 55:383–391

    Article  CAS  PubMed  Google Scholar 

  • Lee HJ, Ryu D (2015) Advances in mycotoxin research: public health perspectives. J Food Sci 80:T2970–83. doi:10.1111/1750-3841.13156

    Article  CAS  PubMed  Google Scholar 

  • Lee RJ, Workman AD, Carey RM et al. (2016) Fungal aflatoxins reduce respiratory mucosal ciliary function. Sci Rep 6:33221. doi:10.1038/srep33221

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leong YH, Rosma A, Latiff AA et al. (2012) Associations of serum aflatoxin B1-lysine adduct level with socio-demographic factors and aflatoxins intake from nuts and related nut products in Malaysia. Int J Hyg Environ Health 215:368–372. doi:10.1016/j.ijheh.2011.12.005

    Article  CAS  PubMed  Google Scholar 

  • Li M, Harkema JR, Cuff CF et al. (2007) Deoxynivalenol exacerbates viral bronchopneumonia induced by respiratory reovirus infection. Toxicol Sci 95:412–426

    Article  CAS  PubMed  Google Scholar 

  • Li M, Harkema JR, Islam Z et al. (2006) T-2 toxin impairs murine immune response to respiratory reovirus and exacerbates viral bronchiolitis. Toxicol Appl Pharmacol 217:76–85. S0041-008X(06)00265-1 [pii]

    Article  CAS  PubMed  Google Scholar 

  • Lichtenstein JH, Molina RM, Donaghey TC et al. (2010) Pulmonary responses to Stachybotrys chartarum and its toxins: mouse strain affects clearance and macrophage cytotoxicity. Toxicol Sci 116:113–121. doi:10.1093/toxsci/kfq104

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lieberman SM, Jacobs JB, Lebowitz RA et al. (2011) Measurement of mycotoxins in patients with chronic rhinosinusitis. Otolaryngol Head Neck Surg 145:327–329. doi:10.1177/0194599811403891

    Article  PubMed  Google Scholar 

  • Louria DB, Finkel G, Smith JK et al. (1974) Aflatoxin-induced tumors in mice. Sabouraudia 12:371–375

    Article  CAS  PubMed  Google Scholar 

  • Malik A, Ali S, Shahid M et al. (2014) Occupational exposure to Aspergillus and aflatoxins among food-grain workers in India. Int J Occup Environ Health 20:189–193. doi:10.1179/2049396714Y.0000000055

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Malir F, Ostry V, Pfohl-Leszkowicz A et al. (2016) Ochratoxin A: 50 years of research. Toxins 8:191. doi:10.3390/toxins8070191

    Article  PubMed Central  CAS  Google Scholar 

  • Marrs TC, Edginton JA, Price PN et al. (1986) Acute toxicity of T2 mycotoxin to the guinea-pig by inhalation and subcutaneous routes. Br J Exp Pathol 67:259–268

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mayer S, Curtui V, Usleber E et al. (2007) Airborne mycotoxins in dust from grain elevators. Mycotoxin Res 23:94–100. doi:10.1007/BF02946033

    Article  CAS  PubMed  Google Scholar 

  • Mayer S, Engelhart S, Kolk A et al. (2008) The significance of mycotoxins in the framework of assessing workplace related risks. Mycotoxin Res 24:151–164. doi:10.1007/BF03032342

    Article  CAS  PubMed  Google Scholar 

  • McIntyre BA, Kushwah R, Mechael R et al. (2015) Innate immune response of human pluripotent stem cell-derived airway epithelium. Innate Immun 21:504–511. doi:10.1177/1753425914551074

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Miller JD, Sun M, Gilyan A et al. (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. doi:10.1016/j.cbi.2009.09.023

    Article  CAS  PubMed  Google Scholar 

  • Mo X, Lai H, Yang Y et al. (2014) How does airway exposure of aflatoxin B1 affect serum albumin adduct concentrations? Evidence based on epidemiological study and animal experimentation. J Toxicol Sci 39:645–653. DN/JST.JSTAGE/jts/39.645 [pii]

    Article  CAS  PubMed  Google Scholar 

  • Munro IC, Renwick AG, Danielewska-Nikiel B (2008) The Threshold of Toxicological Concern (TTC) in risk assessment. Toxicol Lett 180:151–156. doi:10.1016/j.toxlet.2008.05.006

    Article  CAS  PubMed  Google Scholar 

  • Nevalainen A, Täubel M, Hyvärinen A (2015) Indoor fungi: companions and contaminants. Indoor Air 25:125–156. doi:10.1111/ina.12182

    Article  CAS  PubMed  Google Scholar 

  • Niculita-Hirzel H, Hantier G, Storti F et al. (2016) Frequent occupational exposure to Fusarium mycotoxins of workers in the Swiss Grain Industry. Toxins (Basel). 8(12). doi:10.3390/toxins8120370

  • Nielsen KF, Huttunen K, Hyvärinen A et al. (2002) Metabolite profiles of Stachybotrys isolates from water-damaged buildings and their induction of inflammatory mediators and cytotoxicity in macrophages. Mycopathologia 154:201–205

    Article  CAS  PubMed  Google Scholar 

  • Norbäck D, Hashim JH, Cai GH et al. (2016) Rhinitis, ocular, throat and dermal symptoms, headache and tiredness among students in schools from Johor Bahru, Malaysia: associations with fungal DNA and mycotoxins in classroom dust. PLoS One 11:e0147996. doi:10.1371/journal.pone.0147996

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Oluwafemi F, Odebiyi T, Kolapo A (2012) Occupational aflatoxin exposure among feed mill workers in Nigeria. World Mycotoxin J 5:385–389

    Article  CAS  Google Scholar 

  • Pang VF, Lambert RJ, Felsburg PJ et al. (1987) Experimental T-2 toxicosis in swine following inhalation exposure: effects on pulmonary and systemic immunity, and morphologic changes. Toxicol Pathol 15:308–319

    Article  CAS  PubMed  Google Scholar 

  • Pang VF, Lambert RJ, Felsburg PJ et al. (1988) Experimental T-2 toxicosis in swine following inhalation exposure: clinical signs and effects on hematology, serum biochemistry, and immune response. Fundam Appl Toxicol 11:100–109

    Article  CAS  PubMed  Google Scholar 

  • Peitzsch M, Sulyok M, Täubel M et al. (2012) Microbial secondary metabolites in school buildings inspected for moisture damage in Finland, The Netherlands and Spain. J Environ Monit 14:2044–2053. doi:10.1039/c2em30195d

    Article  CAS  PubMed  Google Scholar 

  • Penttinen P, Pelkonen J, Huttunen K et al. (2005) Interactions between Streptomyces californicus and Stachybotrys chartarum can induce apoptosis and cell cycle arrest in mouse RAW264.7 macrophages. Toxicol Appl Pharmacol 202:278–288. S0041-008X(04)00347-3 [pii]

    Article  CAS  PubMed  Google Scholar 

  • Pestka JJ (2010a) Deoxynivalenol: mechanisms of action, human exposure, and toxicological relevance. Arch Toxicol 84:663–679. doi:10.1007/s00204-010-0579-8

    Article  CAS  PubMed  Google Scholar 

  • Pestka JJ (2010b) Deoxynivalenol-induced proinflammatory gene expression: mechanisms and pathological sequelae. Toxins 2:1300–1317. doi:10.3390/toxins2061300

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pestka JJ, Yike I, Dearborn DG et al. (2008) Stachybotrys chartarum, trichothecene mycotoxins, and damp building-related illness: new insights into a public health enigma. Toxicol Sci 104:4–26. doi:10.1093/toxsci/kfm284

    Article  CAS  PubMed  Google Scholar 

  • Pestka JJ, Zhou HR, Moon Y et al. (2004) Cellular and molecular mechanisms for immune modulation by deoxynivalenol and other trichothecenes: unraveling a paradox. Toxicol Lett 153:61–73. doi:10.1016/j.toxlet.2004.04.023

    Article  CAS  PubMed  Google Scholar 

  • Piecková E, Kunová Z (2002) Indoor fungi and their ciliostatic metabolites. Ann Agric Environ Med 9:59–63

    PubMed  Google Scholar 

  • Pinton P, Oswald IP (2014) Effect of deoxynivalenol and other Type B trichothecenes on the intestine: a review. Toxins 6:1615–1643. doi:10.3390/toxins6051615

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Polizzi V, Delmulle B, Adams A et al. (2009) JEM Spotlight: fungi, mycotoxins and microbial volatile organic compounds in mouldy interiors from water-damaged buildings. J Environ Monit 11:1849–1858. doi:10.1039/b906856b

    Article  CAS  PubMed  Google Scholar 

  • Prytherch Z, Job C, Marshall H et al. (2011) Tissue-specific stem cell differentiation in an in vitro airway model. Macromol Biosci 11:1467–1477. doi:10.1002/mabi.201100181

    CAS  PubMed  Google Scholar 

  • Prytherch ZC, BéruBé KA (2014) A normal and biotransforming model of the human bronchial epithelium for the toxicity testing of aerosols and solubilised substances. Altern Lab Anim 42:377–381

    PubMed  Google Scholar 

  • Rand TG, Dipenta J, Robbins C et al. (2011) Effects of low molecular weight fungal compounds on inflammatory gene transcription and expression in mouse alveolar macrophages. Chem Biol Interact 190:139–147. doi:10.1016/j.cbi.2011.02.017

    Article  CAS  PubMed  Google Scholar 

  • Rand TG, Flemming J, David Miller J et al. (2006) Comparison of inflammatory responses in mouse lungs exposed to atranones A and C from Stachybotrys chartarum. J Toxicol Environ Health A 69:1239–1251. R5048J37649XT10X [pii]

    Article  CAS  PubMed  Google Scholar 

  • Rand TG, Giles S, Flemming J et al. (2005) Inflammatory and cytotoxic responses in mouse lungs exposed to purified toxins from building isolated Penicillium brevicompactum Dierckx and P. chrysogenum Thom. Toxicol Sci 87:213–222. doi: kfi223 [pii]

    Article  CAS  PubMed  Google Scholar 

  • Rea WJ, Didriksen N, Simon TR et al. (2003) Effects of toxic exposure to molds and mycotoxins in building-related illnesses. Arch Environ Health 58:399–405

    Article  CAS  PubMed  Google Scholar 

  • REACH (2006) Regulation (EC) no 1907/2006 of the European Parliament and of the Council concerning the Registration, Evaluation, Authorisation and Restriction of Chemicals (REACH). Off J Eur Union L396:1–849

    Google Scholar 

  • Robbins CA, Swenson LJ, Nealley ML et al. (2000) Health effects of mycotoxins in indoor air: a critical review. Appl Occup Environ Hyg 15:773–784. doi:10.1080/10473220050129419

    Article  CAS  PubMed  Google Scholar 

  • Sahlberg B, Gunnbjörnsdottir M, Soon A et al. (2013) Airborne molds and bacteria, microbial volatile organic compounds (MVOC), plasticizers and formaldehyde in dwellings in three North European cities in relation to sick building syndrome (SBS). Sci Total Environ 444:433–40. doi:10.1016/j.scitotenv.2012.10.114

    Article  CAS  PubMed  Google Scholar 

  • Schütze N, Lehmann I, Bönisch U et al. (2010) Exposure to mycotoxins increases the allergic immune response in a murine asthma model. Am J Respir Crit Care Med 181:1188–1199. doi:10.1164/rccm.200909-1350OC

    Article  PubMed  CAS  Google Scholar 

  • Å egvić Klarić M, JakÅ¡ić Despot D, Kopjar N et al. (2015) Cytotoxic and genotoxic potencies of single and combined spore extracts of airborne OTA-producing and OTA-non-producing Aspergilli in human lung A549 cells. Ecotoxicol Environ Saf 120:206–214. doi:10.1016/j.ecoenv.2015.06.002

    Article  PubMed  CAS  Google Scholar 

  • Seifert SA, Von Essen S, Jacobitz K et al. (2003) Organic dust toxic syndrome: a review. J Toxicol Clin Toxicol 41:185–193

    Article  CAS  PubMed  Google Scholar 

  • Selim MI, Juchems AM, Popendorf W (1998) Assessing airborne aflatoxin B1 during on-farm grain handling activities. Am Ind Hyg Assoc J 59:252–256. doi:10.1080/15428119891010514

    Article  CAS  PubMed  Google Scholar 

  • Skaug MA, Eduard W, Stormer FC (2001) Ochratoxin A in airborne dust and fungal conidia. Mycopathologia 151:93–98

    Article  CAS  PubMed  Google Scholar 

  • Sorenson WG, Jones W, Simpson J et al. (1984) Aflatoxin in respirable airborne peanut dust. J Toxicol Environ Health 14:525–533. doi:10.1080/15287398409530603

    Article  CAS  PubMed  Google Scholar 

  • Stoev SD (2015) Foodborne mycotoxicoses, risk assessment and underestimated hazard of masked mycotoxins and joint mycotoxin effects or interaction. Environ Toxicol Pharmacol 39:794–809. doi:10.1016/j.etap.2015.01.022

    Article  CAS  PubMed  Google Scholar 

  • Straus DC (2009) Molds, mycotoxins, and sick building syndrome. Toxicol Ind Health 25:617–635. doi:10.1177/0748233709348287

    Article  CAS  PubMed  Google Scholar 

  • Täubel M, Hyvärinen A (2015) Occurrence of mycotoxins in indoor environments. In: Viegas C, Pinheiro A, Sabino R, et al (eds) Environmental mycology in public health, Amsterdam, Elsevier Academic Press pp 299–319

    Google Scholar 

  • Täubel M, Sulyok M, Vishwanath V et al. (2011) Co-occurrence of toxic bacterial and fungal secondary metabolites in moisture-damaged indoor environments. Indoor Air 21:368–375. doi:10.1111/j.1600-0668.2011.00721.x

    Article  PubMed  CAS  Google Scholar 

  • Thrasher JD, Gray MR, Kilburn KH et al. (2012) A water-damaged home and health of occupants: a case study. J Environ Public Health 2012:312836. doi:10.1155/2012/312836

    Article  PubMed  CAS  Google Scholar 

  • Trout D, Bernstein J, Martinez K et al. (2001) Bioaerosol lung damage in a worker with repeated exposure to fungi in a water-damaged building. Environ Health Perspect 109:641–644. sc271_5_1835 [pii]

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tuomi T, Reijula K, Johnsson T et al. (2000) Mycotoxins in crude building materials from water-damaged buildings. Appl Environ Microbiol 66:1899–1904

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ueno Y (1984) Toxicological features of T-2 toxin and related trichothecenes. Fundam Appl Toxicol 4:S124–32

    Article  CAS  PubMed  Google Scholar 

  • Van Emon JM, Reed AW, Yike I et al. (2003) ELISA measurement of stachylysin in serum to quantify human exposures to the indoor mold Stachybotrys chartarum. J Occup Environ Med 45:582–591. doi:10.1097/01.jom.0000071503.96740.65

    Article  PubMed  CAS  Google Scholar 

  • Van Vleet TR, Klein PJ, Coulombe Jr RA (2001) Metabolism of aflatoxin B1 by normal human bronchial epithelial cells. J Toxicol Environ Health A 63:525–540. doi:10.1080/15287390152410156

    Article  PubMed  Google Scholar 

  • Vejdovszky K, Hahn K, Braun D, et al. (2017) Synergistic estrogenic effects of Fusarium and Alternaria mycotoxins in vitro. Arch Toxicol 91:1147–1460. doi:10.1007/s00204-016-1795-7

    Article  CAS  Google Scholar 

  • Vettorazzi A, van Delft J, López de Cerain A (2013) A review on ochratoxin A transcriptomic studies. Food Chem Toxicol 59:766–783. doi:10.1016/j.fct.2013.05.043

    Article  CAS  PubMed  Google Scholar 

  • Viegas S, Veiga L, Almeida A et al. (2016) Occupational exposure to aflatoxin B1 in a Portuguese poultry slaughterhouse. Ann Occup Hyg 60:176–183. doi:10.1093/annhyg/mev077

    Article  PubMed  Google Scholar 

  • Viegas S, Veiga L, Figueiredo P et al. (2015) Assessment of workers’ exposure to aflatoxin B1 in a Portuguese waste industry. Ann Occup Hyg 59:173–181. doi:10.1093/annhyg/meu082

    PubMed  Google Scholar 

  • Viegas S, Faisca VM, Dias H et al. (2013a) Occupational exposure to poultry dust and effects on the respiratory system in workers. J Toxicol Environ Health A 76:230–239. doi:10.1080/15287394.2013.757199

    Article  CAS  PubMed  Google Scholar 

  • Viegas S, Veiga L, Figueredo P et al. (2013b) Occupational exposure to aflatoxin B1 in swine production and possible contamination sources. J Toxicol Environ Health A 76:944–951. doi:10.1080/15287394.2013.826569

    Article  CAS  PubMed  Google Scholar 

  • Viegas S, Veiga L, Figueredo P et al. (2013c) Occupational exposure of aflatoxin B1: the case of poultry and swine production. World Mycotoxin J 6:309–315

    Article  CAS  Google Scholar 

  • Viegas S, Veiga L, Malta-Vacas J et al. (2012) Occupational exposure to aflatoxin (AFB(1)) in poultry production. J Toxicol Environ Health A 75:1330–1340. doi:10.1080/15287394.2012.721164

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Chai T, Lu G et al. (2008) Simultaneous detection of airborne aflatoxin, ochratoxin and zearalenone in a poultry house by immunoaffinity clean-up and high-performance liquid chromatography. Environ Res 107:139–144. doi:10.1016/j.envres.2008.01.008

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Yike I, Dearborn DG (2004) Pulmonary effects of Stachybotrys chartarum in animal studies. Adv Appl Microbiol 55:241–273. doi:10.1016/S0065-2164(04)55009-8

    Article  CAS  PubMed  Google Scholar 

  • Yike I, Distler AM, Ziady AG et al. (2006) Mycotoxin adducts on human serum albumin: biomarkers of exposure to Stachybotrys chartarum. Environ Health Perspect 114:1221–1226

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yike I, Rand TG, Dearborn DG (2005) Acute inflammatory responses to Stachybotrys chartarum in the lungs of infant rats: time course and possible mechanisms. Toxicol Sci 84:408–417

    Article  CAS  PubMed  Google Scholar 

  • Zarba A, Hmieleski R, Hemenway DR et al. (1992) Aflatoxin B1 – DNA adduct formation in rat liver following exposure by aerosol inhalation. Carcinogenesis 13:1031–1033

    Article  CAS  PubMed  Google Scholar 

  • Zhou HR, Harkema JR, Yan D et al. (1999) Amplified proinflammatory cytokine expression and toxicity in mice coexposed to lipopolysaccharide and the trichothecene vomitoxin (deoxynivalenol). J Toxicol Environ Health A 57:115–136

    Article  CAS  PubMed  Google Scholar 

  • Zock JP, Borras-Santos A, Jacobs J, et al (2014) Dampness and microbial secondary metabolites in schools and respiratory symptoms in teachers. European Respiratory Society 2014 International Congress. Abstract 2161

    Google Scholar 

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Authors and Affiliations

  1. University of Eastern Finland, Department of Environmental and Biological Sciences, Kuopio, Finland

    Kati Huttunen

  2. National Institute for Health and Welfare, Environmental Health Unit, Kuopio, Finland

    Merja Korkalainen

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  1. Kati Huttunen
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  2. Merja Korkalainen
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Correspondence to Kati Huttunen .

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  1. Lisbon School of Health Technology Environment and Health RG, Polytechnic Institute of Lisbon, Lisbon, Portugal

    Carla Viegas

  2. Lisbon School of Health Technology Environment and Health RG, Polytechnic Institute of Lisbon, Lisbon, Portugal

    Susana Viegas

  3. Lisbon School of Health Technology Polytechnic Institute of Lisbon, University of Lisbon, Lisbon, Portugal

    Anita Gomes

  4. Department Health Protection, National Institute for Health & Welfare, Kuopio, Finland

    Martin Täubel

  5. National Health Institute Portugal, Lisbon, Portugal

    Raquel Sabino

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Huttunen, K., Korkalainen, M. (2017). Microbial Secondary Metabolites and Knowledge on Inhalation Effects. In: Viegas, C., Viegas, S., Gomes, A., Täubel, M., Sabino, R. (eds) Exposure to Microbiological Agents in Indoor and Occupational Environments. Springer, Cham. https://doi.org/10.1007/978-3-319-61688-9_10

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