Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Vishniacozyma victoriae (syn. Cryptococcus victoriae) in the homes of asthmatic and non-asthmatic children in New York City

Abstract

Background

Indoor environments contain a broad diversity of non-pathogenic Basidiomycota yeasts, but their role in exacerbating adverse health effects has remained unclear.

Objective

To understand the role of Vishniacozyma victoriae exposure and its impact on human health.

Methods

A qPCR assay was developed to detect and quantify an abundant indoor yeast species, Vishniacozyma victoriae (syn. Cryptococcus victoriae), from homes participating in the New York City Neighborhood Asthma and Allergy Study (NAAS). We evaluated the associations between V. victoriae, housing characteristics, and asthma relevant health endpoints.

Results

V. victoriae was quantified in 236 of the 256 bedroom floor dust samples ranging from less than 300–45,918 cell equivalents/mg of dust. Higher concentrations of V. victoriae were significantly associated with carpeted bedroom floors (P = 0.044), mean specific humidity (P = 0.004), winter (P < 0.0001) and spring (P = 0.001) seasons, and the presence of dog (P = 0.010) and dog allergen Can f 1 (P = 0.027). V. victoriae concentrations were lower in homes of children with asthma vs. without asthma (P = 0.027), an association observed only among the non-seroatopic children.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: V. victoriae standard curve development and distribution.
Fig. 2: Association of V. victoriae with asthma.

Similar content being viewed by others

Antoni Torres, Catia Cilloniz, … Tom van der Poll

References

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

    Article  PubMed  PubMed Central  Google Scholar 

  2. Green BJ, Summerbell RC. Aerosolized fungal fragments. In: Samson RA, Adan OCG (eds). Fundamentals of mold growth in indoor environments and strategies for healthy living. The Netherlands: Wageningen Academic Publishers; 2011.

  3. Ege MJ, Mayer M, Normand AC, Genuneit J, Cookson WO, Braun-Fahrlander C, et al. Exposure to environmental microorganisms and childhood asthma. N Engl J Med. 2011;364:701–9.

    Article  CAS  PubMed  Google Scholar 

  4. Adams RI, Miletto M, Taylor JW, Bruns TD. The diversity and distribution of fungi on residential surfaces. PLoS ONE. 2013;8:e78866.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Sharpe RA, Bearman N, Thornton CR, Husk K, Osborne NJ. Indoor fungal diversity and asthma: a meta-analysis and systematic review of risk factors. J Allergy Clin Immunol. 2015;135:110–22.

    Article  PubMed  Google Scholar 

  6. Park JH, Cox-Ganser JM, Kreiss K, White SK, Rao CY. Hydrophilic fungi and ergosterol associated with respiratory illness in a water-damaged building. Environ Health Perspect. 2008;116:45–50.

    Article  PubMed  Google Scholar 

  7. Ahmadi B, Mirhendi H, Shidfar MR, Nouripour-Sisakht S, Jalalizand N, Geramishoar M, et al. A comparative study on morphological versus molecular identification of dermatophyte isolates. J Mycol Med. 2015;25:29–35.

    Article  CAS  PubMed  Google Scholar 

  8. Rittenour WR, Ciaccio CE, Barnes CS, Kashon ML, Lemons AR, Beezhold DH, et al. Internal transcribed spacer rRNA gene sequencing analysis of fungal diversity in Kansas City indoor environments. Environ Sci Process Impacts. 2014;16:33–43.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL, Levesque CA, et al. Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proc Natl Acad Sci USA. 2012;109:6241–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Dannemiller KC, Mendell MJ, Macher JM, Kumagai K, Bradman A, Holland N, et al. Next-generation DNA sequencing reveals that low fungal diversity in house dust is associated with childhood asthma development. Indoor Air. 2014;24:236–47.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Lemons AR, Hogan MB, Gault RA, Holland K, Sobek E, Olsen-Wilson KA, et al. Microbial rRNA sequencing analysis of evaporative cooler indoor environments located in the Great Basin Desert region of the United States. Environ Sci Process Impacts. 2017;19:101–10.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Hanson B, Zhou Y, Bautista EJ, Urch B, Speck M, Silverman F, et al. Characterization of the bacterial and fungal microbiome in indoor dust and outdoor air samples: a pilot study. Environ Sci Process Impacts. 2016;18:713–24.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Jayaprakash B, Adams RI, Kirjavainen P, Karvonen A, Vepsalainen A, Valkonen M, et al. Indoor microbiota in severely moisture damaged homes and the impact of interventions. Microbiome. 2017;5:138.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Pitkaranta M, Meklin T, Hyvarinen A, Paulin L, Auvinen P, Nevalainen A, et al. Analysis of fungal flora in indoor dust by ribosomal DNA sequence analysis, quantitative PCR, and culture. Appl Environ Microbiol. 2008;74:233–44.

    Article  CAS  PubMed  Google Scholar 

  15. de Garcia V, Zalar P, Brizzio S, Gunde-Cimerman N, van Broock M. Cryptococcus species (Tremellales) from glacial biomes in the southern (Patagonia) and northern (Svalbard) hemispheres. FEMS Microbiol Ecol. 2012;82:523–39.

    Article  PubMed  Google Scholar 

  16. Idnurm A, Lin X. Rising to the challenge of multiple Cryptococcus species and the diseases they cause. Fungal Genet Biol. 2015;78:1–6.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Khawcharoenporn T, Apisarnthanarak A, Mundy LM. Non-neoformans cryptococcal infections: a systematic review. Infection 2007;35:51–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Mondini A, Donhauser J, Itcus C, Marin C, Perșoiu A, Lavin P, et al. High-throughput sequencing of fungal communities across the perennial ice block of Scărișoara Ice Cave. Ann Glaciol. 2018;59:134–46.

    Article  Google Scholar 

  19. Montes MJ, Belloch C, Galiana M, Garcia MD, Andres C, Ferrer S, et al. Polyphasic taxonomy of a novel yeast isolated from antarctic environment; description of Cryptococcus victoriae sp. nov. Syst Appl Microbiol. 1999;22:97–105.

    Article  CAS  PubMed  Google Scholar 

  20. Behbod B, Sordillo JE, Hoffman EB, Datta S, Webb TE, Kwan DL, et al. Asthma and allergy development: contrasting influences of yeasts and other fungal exposures. Clin Exp Allergy. 2015;45:154–63.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Goldman DL, Huffnagle GB. Potential contribution of fungal infection and colonization to the development of allergy. Med Mycol. 2009;47:445–56.

    Article  CAS  PubMed  Google Scholar 

  22. Lin S, Fitzgerald E, Hwang SA, Munsie JP, Stark A. Asthma hospitalization rates and socioeconomic status in New York State (1987-1993). J Asthma. 1999;36:239–51.

    Article  CAS  PubMed  Google Scholar 

  23. Olmedo O, Goldstein IF, Acosta L, Divjan A, Rundle AG, Chew GL, et al. Neighborhood differences in exposure and sensitization to cockroach, mouse, dust mite, cat, and dog allergens in New York City. J Allergy Clin Immunol. 2011;128:284–92.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Environment and Health Data Portal NYC.gov: The City of New York [Asthma Prevalence - Children ever diagnosed with asthma (ages 0-13 years) - Percentage, 2017, Neighborhood (NYC KIDS)]. 2020. http://a816-dohbesp.nyc.gov/IndicatorPublic/VisualizationData.aspx?id=2392,4466a0,11,Map,Percentage,2017.

  25. Mainardi TR, Mellins RB, Miller RL, Acosta LM, Cornell A, Hoepner L, et al. Exercise-induced wheeze, urgent medical visits, and neighborhood asthma prevalence. Pediatrics. 2013;131:e127–35.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Yamamoto N, Bibby K, Qian J, Hospodsky D, Rismani-Yazdi H, Nazaroff WW, et al. Particle-size distributions and seasonal diversity of allergenic and pathogenic fungi in outdoor air. ISME J. 2012;6:1801–11.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Yang RH, Su JH, Shang JJ, Wu YY, Li Y, Bao DP, et al. Evaluation of the ribosomal DNA internal transcribed spacer (ITS), specifically ITS1 and ITS2, for the analysis of fungal diversity by deep sequencing. PLoS ONE. 2018;13:e0206428.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Cornell AG, Chillrud SN, Mellins RB, Acosta LM, Miller RL, Quinn JW, et al. Domestic airborne black carbon and exhaled nitric oxide in children in NYC. J Expo Sci Environ Epidemiol. 2012;22:258–66.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Donohue KM, Al-alem U, Perzanowski MS, Chew GL, Johnson A, Divjan A, et al. Anti-cockroach and anti-mouse IgE are associated with early wheeze and atopy in an inner-city birth cohort. J Allergy Clin Immunol. 2008;122:914–20.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Chang C, Gauvey-Kern K, Johnson A, Kelvin EA, Chew GL, Perera F, et al. Cord blood versus age 5 mononuclear cell proliferation on IgE and asthma. Clin Mol Allergy. 2010;8:11.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Tamerius J, Perzanowski M, Acosta L, Jacobson J, Goldstein I, Quinn J, et al. Socioeconomic and outdoor meteorological determinants of indoor temperature and humidity in New York city dwellings. Weather Clim Soc. 2013;5:168–79.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Eder W, Ege MJ, von Mutius E. The asthma epidemic. N Engl J Med. 2006;355:2226–35.

    Article  CAS  PubMed  Google Scholar 

  33. Vesper S, McKinstry C, Haugland R, Wymer L, Bradham K, Ashley P, et al. Development of an environmental relative moldiness index for US homes. J Occup Environ Med. 2007;49:829–33.

    Article  PubMed  Google Scholar 

  34. Goldman DL, Davis J, Bommarito F, Shao X, Casadevall A. Enhanced allergic inflammation and airway responsiveness in rats with chronic Cryptococcus neoformans infection: potential role for fungal pulmonary infection in the pathogenesis of asthma. J Infect Dis. 2006;193:1178–86.

    Article  CAS  PubMed  Google Scholar 

  35. Siggins A, Gunnigle E, Abram F. Exploring mixed microbial community functioning: recent advances in metaproteomics. FEMS Microbiol Ecol. 2012;80:265–80.

    Article  CAS  PubMed  Google Scholar 

  36. Brankatschk R, Bodenhausen N, Zeyer J, Bürgmann H. Simple absolute quantification method correcting for quantitative PCR efficiency variations for microbial community samples. Appl Environ Microbiol. 2012;78:4481–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Dannemiller KC, Gent JF, Leaderer BP, Peccia J. Influence of housing characteristics on bacterial and fungal communities in homes of asthmatic children. Indoor Air. 2016;26:179–92.

    Article  CAS  PubMed  Google Scholar 

  38. Foster ML, Dowd SE, Stephenson C, Steiner JM, Suchodolski JS. Characterization of the fungal microbiome (mycobiome) in fecal samples from dogs. Vet Med Int. 2013;2013:658373.

    Article  PubMed  PubMed Central  Google Scholar 

  39. Chermprapai S, Ederveen THA, Broere F, Broens EM, Schlotter YM, van Schalkwijk S, et al. The bacterial and fungal microbiome of the skin of healthy dogs and dogs with atopic dermatitis and the impact of topical antimicrobial therapy, an exploratory study. Vet Microbiol. 2019;229:90–9.

    Article  CAS  PubMed  Google Scholar 

  40. Campo P, Kalra HK, Levin L, Reponen T, Olds R, Lummus ZL, et al. Influence of dog ownership and high endotoxin on wheezing and atopy during infancy. J Allergy Clin Immunol. 2006;118:1271–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Ownby DR, Johnson CC, Peterson EL. Exposure to dogs and cats in the first year of life and risk of allergic sensitization at 6 to 7 years of age. JAMA. 2002;288:963–72.

    Article  PubMed  Google Scholar 

  42. Fujimura KE, Demoor T, Rauch M, Faruqi AA, Jang S, Johnson CC, et al. House dust exposure mediates gut microbiome Lactobacillus enrichment and airway immune defense against allergens and virus infection. Proc Natl Acad Sci USA. 2014;111:805–10.

    Article  CAS  PubMed  Google Scholar 

  43. Fujimura KE, Johnson CC, Ownby DR, Cox MJ, Brodie EL, Havstad SL, et al. Man’s best friend? The effect of pet ownership on house dust microbial communities. J Allergy Clin Immunol. 2010;126:410–2.

    Article  PubMed  PubMed Central  Google Scholar 

  44. Kitagaki K, Businga TR, Racila D, Elliott DE, Weinstock JV, Kline JN. Intestinal helminths protect in a murine model of asthma. J Immunol. 2006;177:1628–35.

    Article  CAS  PubMed  Google Scholar 

  45. Parande Shirvan S, Ebrahimby A, Dousty A, Maleki M, Movassaghi A, Borji H, et al. Somatic extracts of Marshallagia marshalli downregulate the Th2 associated immune responses in ovalbumin-induced airway inflammation in BALB/c mice. Parasit Vectors. 2017;10:233.

    Article  PubMed  PubMed Central  Google Scholar 

  46. Preston JA, Thorburn AN, Starkey MR, Beckett EL, Horvat JC, Wade MA, et al. Streptococcus pneumoniae infection suppresses allergic airways disease by inducing regulatory T-cells. Eur Respir J. 2011;37:53–64.

    Article  CAS  PubMed  Google Scholar 

  47. Ober C, Sperling AI, von Mutius E, Vercelli D. Immune development and environment: lessons from Amish and Hutterite children. Curr Opin Immunol. 2017;48:51–60.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Hedman J, Radstrom P. Overcoming inhibition in real-time diagnostic PCR. Methods Mol Biol. 2013;943:17–48.

    Article  CAS  PubMed  Google Scholar 

  49. Vesper SJ, Wymer LJ, Meklin T, Varma M, Stott R, Richardson M, et al. Comparison of populations of mould species in homes in the UK and USA using mould-specific quantitative PCR. Lett Appl Microbiol. 2005;41:367–73.

    Article  CAS  PubMed  Google Scholar 

  50. Haugland RA, Brinkman N, Vesper SJ. Evaluation of rapid DNA extraction methods for the quantitative detection of fungi using real-time PCR analysis. J Microbiol Methods. 2002;50:319–23.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors would like to acknowledge Angela Lemons for her assistance with techniques and manuscript preparation. We would like to thank the NYC Neighborhood Asthma and Allergy Study field team for their hard work. We would also like to thank the families who have participated in the study. The findings and conclusions in this study are those of the authors and do not necessarily represent the official position of the National Institute for Occupational Safety and Health, Centers for Disease Control and Prevention.

Funding

This study was supported in part by an interagency agreement between NIOSH and NIEHS (AES 12007001-1-0-6) as a collaborative National Toxicology Program research activity. This study was supported by the National Institute of Environmental Health Sciences (NIEHS) [grant #’s R01 ES014400, P30 ES09089] the Department of Housing and Urban Development (HUD) Healthy Homes, and Lead Technical Study [HUD NYHHU0003-11, NYHHU0021-13].

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Brett J. Green.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rush, R.E., Dannemiller, K.C., Cochran, S.J. et al. Vishniacozyma victoriae (syn. Cryptococcus victoriae) in the homes of asthmatic and non-asthmatic children in New York City. J Expo Sci Environ Epidemiol 32, 48–59 (2022). https://doi.org/10.1038/s41370-021-00342-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41370-021-00342-4

Keywords

Search

Quick links