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Fungi and Atopy

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Abstract

Atopy and fungi have a long associative history. Fungal spores were among the first substances to which humans were noted to be sensitized. Humans contact fungal spores in the outdoor, indoor, and occupational environments. As organisms, fungi have their own kingdom and are found in all environmental niches on earth. Currently, fungal exposure in the indoor environment especially related to wet housing conditions is of particular concern. Sensitization rates to fungi typically exceed 5% of the general public with higher rates among the atopic population. Alternaria is the best studied of the allergic fungi; however, cross sensitization to multiple fungi is well documented. Recent advances in understanding mechanisms of the innate immune system are beginning to explain why the fungal atopy relationship is unique and why fungal sensitivity seems to extend to many non-atopic individuals. Evidence has been accumulated that indicates fungal allergen exposure can be via intact spores as well as spore and mycelial fragments. Germinating spores produce a different and often increased allergen picture. Much evidence has been developed through animal studies that extends the mechanisms surrounding long-term low-level fungal exposure. However, it should be emphasized that the presence of fungi in the air does not necessarily equate with illness. Indeed, in the absence of an atopic individual and/or a significant immune response against fungi, there is little evidence suggesting pathology. Allergists frequently deal with patients who have concerns about indoor fungal exposure and respiratory disease in those patients with an allergic response.

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References

  1. Blackly C (1873) Experimental researches on the causes and nature of catarrher aestirus (Hay fever and Hay asthma). Balliere, Tindall and Cox, London

    Google Scholar 

  2. Walton CH (1949) Respiratory allergy due to fungi. Can Med Assoc J 60(3):272–275

    CAS  PubMed  PubMed Central  Google Scholar 

  3. Feinberg SM (1944) Allergy in practice. Year Book Publ, Chicago

    Google Scholar 

  4. Warner JO, Taylor BW, Norman AP, Soothill JF (1976) Association of cystic fibrosis with allergy. Arch Dis Child 51(7):507–511

    CAS  PubMed  PubMed Central  Google Scholar 

  5. Nelson LA, Callerame ML, Schwartz RH (1979) Aspergillosis and atopy in cystic fibrosis. Am Rev Respir Dis 120(4):863–873

    CAS  PubMed  Google Scholar 

  6. Institute of Medicine (US) Committee on Damp Indoor Spaces and Health (2004) Damp indoor spaces and health. National Academies Press (US), Washington (DC)

    Google Scholar 

  7. Sheehan WJ, Gaffin JM, Peden DB, Bush RK, Phipatanakul W (2017) Advances in environmental and occupational disorders in 2016. J Allergy Clin Immunol 140(6):1683–1692

    PubMed  PubMed Central  Google Scholar 

  8. Knutsen AP, Slavin RG (2011) Allergic bronchopulmonary aspergillosis in asthma and cystic fibrosis. Clin Dev Immunol 2011:843763

    PubMed  PubMed Central  Google Scholar 

  9. Whittaker RH (1969) New concepts of kingdoms of organisms. Science 163:150–160

    CAS  PubMed  Google Scholar 

  10. Kendrick B (2001) The fifth kingdom, 3rd edn. Focus Publishing/R. Pullins Co., ASIN: B00ME3Y534

  11. Levetin E, Horner WE, Scott JA (2016) Environmental allergens workgroup. taxonomy of allergenic fungi. J Allergy Clin Immunol Pract 4(3):375–385

    PubMed  Google Scholar 

  12. National Academies of Sciences, Engineering, and Medicine; National Academy of Engineering; Division on Engineering and Physical Sciences; Health and Medicine Division; Division on Earth and Life Studies; Board on Infrastructure and the Constructed Environment; Board on Environmental Studies and Toxicology; Board on Life Sciences; Committee on Microbiomes of the Built Environment: From Research to Application (2017) Microbiomes of the Built Environment: A Research Agenda for Indoor Microbiology, Human Health, and Buildings. National Academies Press (US); Aug. The National Academies Collection: Reports funded by National Institutes of Health. Washington (DC)

  13. de Boer W, Folman LB, Summerbell RC, Boddy L (2005) Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiol Rev 29(4):795–811

    PubMed  Google Scholar 

  14. Yafetto L, Carroll L, Cui Y, Davis DJ, Fischer MW, Henterly AC, Kessler JD, Kilroy HA, Shidler JB, Stolze-Rybczynski JL, Sugawara Z, Money NP (2008) The fastest flights in nature: high-speed spore discharge mechanisms among fungi. PLoS One 3(9):e3237. https://doi.org/10.1371/journal.pone.0003237

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Nature, Spore Dissemination through the Upper Atmosphere. Nature. 1932/05/21/online 129:754

  16. Salo PM, Arbes SJ Jr, Jaramillo R, Calatroni A, Weir CH, Sever ML, Hoppin JA, Rose KM, Liu AH, Gergen PJ, Mitchell HE, Zeldin DC (2014) Prevalence of allergic sensitization in the United States: results from the National Health and Nutrition Examination Survey (NHANES) 2005-2006. J Allergy Clin Immunol 134(2):350–359

    PubMed  PubMed Central  Google Scholar 

  17. Arbes SJ Jr, Gergen PJ, Elliott L, Zeldin DC (2005) Prevalences of positive skin test responses to 10 common allergens in the US population: results from the third National Health and Nutrition Examination Survey. J Allergy Clin Immunol 116(2):377–383 Manuscript Click here to access/download;Manuscript;2 References5.rtf

    PubMed  Google Scholar 

  18. Green BJ, Lemons AR, Park Y, Cox-Ganser JM, Park JH (2017) Assessment of fungal diversity in a water-damaged office building. J Occup Environ Hyg 14(4):285–293

    PubMed  PubMed Central  Google Scholar 

  19. Rittenour WR, Ciaccio CE, Barnes CS, Kashon ML, Lemons AR, Beezhold DH, Green BJ (2014) Internal transcribed spacer rRNA gene sequencing analysis of fungal diversity in Kansas City indoor environments. Environ Sci Process Impacts 16(1):33–43

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Ahluwalia SK, Matsui EC (2018) Indoor environmental interventions for furry pet allergens, pest allergens, and mold: looking to the future. J Allergy Clin Immunol Pract 6(1):9–19

    PubMed  PubMed Central  Google Scholar 

  21. Amado M, Portnoy J Barnes C (2014) J Allergy Clin Immunol 133(2, Supplement):AB92

    Google Scholar 

  22. Williams PB, Barnes CS, Portnoy JM (2016) Environmental allergens workgroup. Innate and adaptive immune response to fungal products and allergens. J Allergy Clin Immunol Pract 4(3):386–395

    PubMed  Google Scholar 

  23. Dobrey AN (1962) Mold sensitivity in the allergic respiratory diseases. Can Med Assoc J 87:1310–1313

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Crameri R, Zeller S, Glaser AG, Vilhelmsson M, Rhyner C (2009) Cross-reactivity among fungal allergens: a clinically relevant phenomenon? Mycoses. 52(2):99–106

    CAS  PubMed  Google Scholar 

  25. O'Neil CE, Horner WE, Reed MA, Lopez M, Lehrer SB (1990) Evaluation of basidiomycete and Deuteromycete (Fungi Imperfecti) extracts for shared allergenic determinants. Clin Exp Allergy 20(5):533–538

    CAS  PubMed  Google Scholar 

  26. De Zubiria A, Horner WE, Lehrer SB (1990) Evidence for cross-reactive allergens among basidiomycetes: immunoprint-inhibition studies. J Allergy Clin Immunol 86(1):26–33

    PubMed  Google Scholar 

  27. Bisht V, Singh BP, Arora N, Gaur SN, Sridhara S (2002) Antigenic and allergenic cross-reactivity of Epicoccum nigrum with other fungi. Ann Allergy Asthma Immunol 89(3):285–291

    CAS  PubMed  Google Scholar 

  28. Crameri R, Weichel M, Fluckiger S, Glaser AG, Rhyner C (2006) Fungal allergies: a yet unsolved problem. Chem Immunol Allergy 91:121–133

    CAS  PubMed  Google Scholar 

  29. O'Hollaren MT, Yunginger JW, Offord KP, Somers MJ, O'Connell EJ, Ballard DJ, Sachs MI (1991) Exposure to an aeroallergen as a possible precipitating factor in respiratory arrest in young patients with asthma. N Engl J Med 324(6):359–363

    CAS  PubMed  Google Scholar 

  30. Lee E, Lee SH, Kim YH, Cho HJ, Yoon J, Yang SI, Jung YH, Kim HY, Seo J, Kwon JW, Kim HB, Lee SY, Kwon HJ, Hong SJ (2017) Association of atopy phenotypes with new development of asthma and bronchial hyperresponsiveness in school-aged children. Ann Allergy Asthma Immunol 118(5):542–550

    PubMed  Google Scholar 

  31. Lehmann S, Sprünken A, Wagner N, Tenbrock K, Ott H (2017) Clinical relevance of IgE-mediated sensitization against the mould Alternaria alternata in children with asthma. Ther Adv Respir Dis 11(1):30–39

    CAS  PubMed  Google Scholar 

  32. Moral L, Roig M, Garde J, Alós A, Toral T, Fuentes MJ (2008) Allergen sensitization in children with asthma and rhinitis: marked variations related to age and microgeographical factors. Allergol Immunopathol (Madr) 36(3):128–133

    CAS  Google Scholar 

  33. Amarsaikhan N, O'Dea EM, Tsoggerel A, Owegi H, Gillenwater J, Templeton SP (2014) Isolate-dependent growth, virulence, and cell wall composition in the human pathogen Aspergillus fumigatus. PLoS One 9(6):e100430

    PubMed  PubMed Central  Google Scholar 

  34. Mitakakis TZ, Barnes C, Tovey ER (2001) Spore germination increases allergen release from Alternaria. J Allergy Clin Immunol 107(2):388–390

    CAS  PubMed  Google Scholar 

  35. Green BJ, Mitakakis TZ, Tovey ER (2003) Allergen detection from 11 fungal species before and after germination. J Allergy Clin Immunol 111(2):285–289

    PubMed  Google Scholar 

  36. Green BJ, Tovey ER, Sercombe JK, Blachere FM, Beezhold DH, Schmechel D (2006) Airborne fungal fragments and allergenicity. Med Mycol 44(Suppl 1):S245–S255

    CAS  PubMed  Google Scholar 

  37. Sercombe JK, Liu-Brennan D, McKay KO, Green BJ, Tovey ER (2014) Domestic exposure to fungal allergenic particles determined by halogen immunoassay using subject's serum versus particles carrying three non-fungal allergens determined by allergen-specific HIA. Indoor Air 24(4):438–445

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Green BJ, Tovey ER, Beezhold DH, Perzanowski MS, Acosta LM, Divjan AI, Chew GL (2009) Surveillance of Fungal Allergic Sensitization Using the Fluorescent Halogen Immunoassay. J Mycol Med 19(4):253–261

    PubMed  PubMed Central  Google Scholar 

  39. Nayak AP, Green BJ, Lemons AR, Marshall N, Goldsmith WT, Kashon ML, Anderson SE, Germolec DR, Beezhold DH (2016) Subchronic exposures to fungal bioaerosols promotes allergic pulmonary inflammation in naïve mice. Clin Exp Allergy 46(6):861–870

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Lee HJ, Ryu D (2015) Advances in mycotoxin research: public health perspectives. J Food Sci 80(12):T2970–T2983

    CAS  PubMed  Google Scholar 

  41. Jarvis BB, Miller JD (2005) Mycotoxins as harmful indoor air contaminants. Appl Microbiol Biotechnol 66(4):367–72.39B

    CAS  PubMed  Google Scholar 

  42. Bennett JW, Klich M (2003) Mycotoxins. Clin Microbiol Rev 16(3):497–516

    CAS  PubMed  PubMed Central  Google Scholar 

  43. (2009) WHO guidelines for indoor air quality: dampness and mould. World Health Organization, Copenhagen. http://www.euro.who.int/__data/assets/pdf_file/0017/43325/E92645.pdf. Accessed 16 July 2019

  44. Gravesen S, Nielsen PA, Iversen R, Nielsen KF (1999) Microfungal contamination of damp buildings--examples of risk constructions and risk materials. Environ Health Perspect 107(Suppl 3):505–508

    PubMed  PubMed Central  Google Scholar 

  45. Barnes C, Buckley S, Pacheco F, Portnoy J (2002) IgE-reactive proteins from Stachybotrys chartarum. Ann Allergy Asthma Immunol 89(1):29–33

    PubMed  Google Scholar 

  46. Shi C, Smith ML, Miller JD (2011) Characterization of human antigenic proteins SchS21 and SchS34 from Stachybotrys chartarum. Int Arch Allergy Immunol 155(1):74–85

    CAS  PubMed  Google Scholar 

  47. Kawamoto M, Page E (2015) Notes from the field: use of unvalidated urine mycotoxin tests for the clinical diagnosis of illness — United States, 2014. MMWR 64(06):157–158 https://www.cdc.gov/mmwr/preview/mmwrhtml/mm6406a7.htm

    PubMed  PubMed Central  Google Scholar 

  48. Portnoy JM, Barnes CS, Kennedy K (2008) Importance of mold allergy in asthma. Curr Allergy Asthma Rep 8(1):71–78

    CAS  PubMed  Google Scholar 

  49. von Mutius E (2016) The microbial environment and its influence on asthma prevention in early life. J Allergy Clin Immunol 137(3):680–689

    Google Scholar 

  50. Heederik D, von Mutius E (2012) Does diversity of environmental microbial exposure matter for the occurrence of allergy and asthma? J Allergy Clin Immunol 130(1):44–50

    PubMed  Google Scholar 

  51. Tischer C, Weikl F, Probst AJ, Standl M, Heinrich J, Pritsch K (2016) Urban dust microbiome: impact on later atopy and wheezing. Environ Health Perspect 124(12):1919–1923

    PubMed  PubMed Central  Google Scholar 

  52. Dannemiller KC, Gent JF, Leaderer BP, Peccia J (2016) Indoor microbial communities: influence on asthma severity in atopic and nonatopic children. J Allergy Clin Immunol. 138(1):76–83

    Google Scholar 

  53. Karvonen AM, Hyvärinen A, Korppi M, Haverinen-Shaughnessy U, Renz H, Pfefferle PI, Remes S, Genuneit J, Pekkanen J (2015) Moisture damage and asthma: a birth cohort study. Pediatrics 135(3):e598–e606

    PubMed  Google Scholar 

  54. Adams RI, Miletto M, Taylor JW, Bruns TD (2013) Dispersal in microbes: Fungi in indoor air are dominated by outdoor air and show dispersal limitation at short distances. ISME J 7:1262–1273

    CAS  PubMed  PubMed Central  Google Scholar 

  55. Jara D, Portnoy J, Dhar M, Barnes C (2017) Relation of indoor and outdoor airborne fungal spore levels in the Kansas City metropolitan area. Allergy Asthma Proc 38(2):130–135. https://doi.org/10.2500/aap.2017.38.4030

    Article  PubMed  Google Scholar 

  56. Horner WE, Barnes C, Codina R, Levetin E (2008) Guide for interpreting reports from inspections/investigations of indoor mold. J Allergy Clin Immunol 121(3):592–597

    PubMed  Google Scholar 

  57. Chew GL, Horner WE, Kennedy K, Grimes C, Barnes CS, Phipatanakul W, Larenas-Linnemann D, Miller JD, Environmental Allergens Workgroup (2016) Procedures to assist health care providers to determine when home assessments for potential mold exposure are warranted. J Allergy Clin Immunol Pract 4(3):417–422

    PubMed  PubMed Central  Google Scholar 

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

    CAS  Google Scholar 

  59. Kercsmar C, Dearborn D, Schluchter M, Xue L, Kirchner HL, Sobolewski J et al (2006) Reduction in asthma morbidity in children as a result of home remediation aimed at moisture sources. Environ Health Perspect 114:1574–1580

    PubMed  PubMed Central  Google Scholar 

  60. 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:S11–S20

    PubMed  PubMed Central  Google Scholar 

  61. Brugge D, Rice PW, Terry P, Howard L, Best J (2001) Housing conditions and respiratory health in a Boston public housing community. New Solut 11:149–164

    CAS  PubMed  Google Scholar 

  62. Barnes CS (2018) Impact of climate change on pollen and respiratory disease. Curr Allergy Asthma Rep 18(11):59

    PubMed  Google Scholar 

  63. Barnes C, Horner WE, Kennedy K, Grimes C, Miller JD (2016) Home assessment and remediation. J Allergy Clin Immunol Pract 4(3):424–431

    Google Scholar 

  64. Barnes CS, Dowling P, Van Osdol T, Portnoy J (2007) Comparison of indoor fungal spore levels before and after professional home remediation. Ann Allergy Asthma Immunol 98(3):262–268

    PubMed  Google Scholar 

  65. Sauni R, Uitti J, Jauhiainen M, Kreiss K, Sigsgaard T, Verbeek JH (2011) Remediating buildings damaged by dampness and mould for preventing or reducing respiratory tract symptoms, infections and asthma. Cochrane Database Syst Rev 9:CD007897

    Google Scholar 

  66. Barnes CS, Kennedy K, Johnson L, Forrest E, Gard L, Pacheco F, Amado M, Portnoy J (2008) Use of dilute sodium hypochlorite spray and home cleaning to reduce indoor allergen levels and improve asthma health parameters. Ann Allergy Asthma Immunol 101:551–552

    PubMed  Google Scholar 

  67. Barnes CS, Kennedy K, Gard L, Forrest E, Johnson L, Pacheco F, Hu F, Amado M, Portnoy JM (2008) The impact of home cleaning on quality of life for homes with asthmatic children. Allergy Asthma Proc 29:197–204

    PubMed  Google Scholar 

  68. 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(6):748–756

    CAS  PubMed  PubMed Central  Google Scholar 

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  1. Allergy, Asthma, Immunology, Children’s Mercy Hospital, Kansas City, MO, USA

    Charles Barnes

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Correspondence to Charles Barnes.

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I am retired from Children’s Mercy Hospital where I am a Professor Emeritus at the University of Missouri – Kansas City School of Medicine. I have no conflicts of interest with regard to this manuscript.

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Barnes, C. Fungi and Atopy. Clinic Rev Allerg Immunol 57, 439–448 (2019). https://doi.org/10.1007/s12016-019-08750-z

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