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Quantitative assessment of microbes from samples of indoor air and dust

Abstract

Different types of house dust samples are widely used as surrogates of airborne inhalation exposure in studies assessing health effects of indoor microbes. Here we studied—in a quantitative assessment—the representativeness of different house dust samples of indoor air (IA) and investigated seasonality and reproducibility of indoor samples. Microbial exposure was measured five times over 1 year in four rural and five urban Finnish homes. Six sampling methods were used: button inhalable aerosol sampler (actively collected personal and indoor air sampling), settled dust, floor dust, mattress dust and vacuum cleaner dust bag dust; the latter three referred to herein as “reservoir dust samples”. Using quantitative PCR, we quantified the fungal species Cladosporium herbarum, the fungal group Penicillium/Aspergillus/Paecilomyces variotii, total fungal DNA, and Gram-positive and Gram-negative bacteria. We observed significant differences in microbial levels between rural and urban homes, most pronounced for personal air samples. Fungal species and groups but not total fungal DNA in indoor air correlated moderately to well with reservoir dust and with personal air samples. For bacterial groups, the correlations between air and dust were generally lower. Samples of indoor air and settled dust reflected similarly seasonal variation in microbial levels and were also similar compositionally, as assessed by ratios of qPCR markers. In general, determinations from mattress dust and other reservoir samples were better reproducible in repeated assessments over time than from indoor air or settled dust. This study indicates that settled dust reflects the microbial composition of indoor air and responds similarly to environmental determinants. Reservoir dusts tend to predict better microbial levels in indoor air and are more reproducible. Sampling strategies in indoor studies need to be developed based on the study questions and may need to rely on more than one type of sample.

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References

  1. Braun-Fahrlander C, Gassner M, Grize L, Neu U, Sennhauser FH, Varonier HS et al. Prevalence of hay fever and allergic sensitization in farmer’s children and their peers living in the same rural community. Clin Exp Allergy 1999; 29: 28–34.

    Article  CAS  Google Scholar 

  2. Ege MJ, Mayer M, Normand AC, Genuneit J, Cookson W, Braun-Fahrlander C et al. Exposure to environmental microorganisms and childhood asthma. N Engl J Med 2011; 364: 701–709.

    Article  CAS  Google Scholar 

  3. von Mutius E, Vercelli D . Farm living: effects on childhood asthma and allergy. Nat Rev Immunol 2010; 10: 861–868.

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  5. Kanchongkittiphon W, Mendell MJ, Gaffin JM, Wang G, Phipatanakul W . Indoor environmental exposures and exacerbation of asthma: an update to the 2000 review by the Institute of Medicine. Environ Health Perspect 2015; 123: 6–20.

    Article  CAS  Google Scholar 

  6. WHO. WHO Guidelines for Indoor Air Quality: Dampness and Mould. WHO Regional Office for Europe: Copenhagen, Denmark, 2009.

  7. Pekkanen J, Hyvarinen A, Haverinen-Shaughnessy U, Korppi M, Putus T, Nevalainen A . Moisture damage and childhood asthma: a population-based incident case-control study. Eur Resp J 2007; 29: 509–515.

    Article  CAS  Google Scholar 

  8. Karvonen AM, Hyvarinen A, Korppi M, Haverinen-Shaughnessy U, Renz H, Pfefferle PI et al. Moisture damage and asthma: a birth cohort study. Pediatrics 2015; 135: E598–E606.

    Article  Google Scholar 

  9. Hyvärinen A, Vahteristo M, Meklin T, Jantunen M, Nevalainen A, Moschandreas D . Temporal and spatial variation of fungal concentrations in indoor air. Aerosol Sci Technol 2001; 35: 688–695.

    Article  Google Scholar 

  10. Institute of Medicine (US) Committee on Damp Indoor Spaces and Health 2004. National Academies of Science, Washington, D.C.

  11. Frankel M, Timm M, Hansen EW, Madsen AM . Comparison of sampling methods for the assessment of indoor microbial exposure. Indoor Air 2012; 22: 405–414.

    Article  CAS  Google Scholar 

  12. Noss I, Wouters IM, Visser M, Heederik DJ, Thorne PS, Brunekreef B et al. Evaluation of a low-cost electrostatic dust fall collector for indoor air endotoxin exposure assessment. Appl Environ Microbiol 2008; 74: 5621–5627.

    Article  CAS  Google Scholar 

  13. Kilburg-Basnyat B, Peters TM, Perry SS, Thorne PS . Electrostatic dust collectors compared to inhalable samplers for measuring endotoxin concentrations in farm homes. Indoor Air 2016; 26: 724–733.

    Article  CAS  Google Scholar 

  14. Hyvärinen A, Roponen M, Tiittanen P, Laitinen S, Nevalainen A, Pekkanen J . Dust sampling methods for endotoxin—an essential, but underestimated issue. Indoor Air 2006; 16: 20–27.

    Article  Google Scholar 

  15. Casas L, Tischer C, Wouters IM, Valkonen M, Gehring U, Doekes G et al. Endotoxin, extracellular polysaccharides, and beta(1-3)-glucan concentrations in dust and their determinants in four European birth cohorts: results from the HITEA project. Indoor Air 2013; 23: 208–218.

    Article  CAS  Google Scholar 

  16. Sordillo JE, Alwis UK, Hoffman E, Gold DR, Milton DK . Home characteristics as predictors of bacterial and fungal microbial biomarkers in house dust. Environ Health Perspect 2011; 119: 189–195.

    Article  CAS  Google Scholar 

  17. Johansson E, Vesper S, Levin L, LeMasters G, Grinshpun S, Reponen T . Streptomycetes in house dust: associations with housing characteristics and endotoxin. Indoor Air 2011; 21: 300–310.

    Article  CAS  Google Scholar 

  18. Frankel M, Beko G, Timm M, Gustavsen S, Hansen EW, Madsen AM . Seasonal variations of indoor microbial exposures and their relation to temperature, relative humidity, and air exchange rate. Appl Environ Microbiol 2012; 78: 8289–8297.

    Article  CAS  Google Scholar 

  19. Heinrich J, Holscher B, Douwes J, Richter K, Koch A, Bischof W et al. Reproducibility of allergen, endotoxin and fungi measurements in the indoor environment. J Exp Anal Environ Epidemiol 2003; 13: 152–160.

    Article  CAS  Google Scholar 

  20. Koch A, Heilemann KJ, Bischof W, Heinrich J, Wichmann HE . Indoor viable mold spores—a comparison between two cities, Erfurt (eastern Germany) and Hamburg (western Germany). Allergy 2000; 55: 176–180.

    Article  CAS  Google Scholar 

  21. Ren P, Jankun TM, Leaderer BP . Comparisons of seasonal fungal prevalence in indoor and outdoor air and in house dusts of dwellings in one Northeast American county. J Exp Anal Environ Epidemiol 1999; 9: 560–568.

    Article  CAS  Google Scholar 

  22. Wu Y, Chan C, Rao CY, Lee, Chung-Te, Hsu, Hsiao-Hsien, Chiu Y, Chao HJ . Characteristics, determinants, and spatial variations of ambient fungal levels in the subtropical. Taipei Metropolis 2007; 41: 2500–2509.

    CAS  Google Scholar 

  23. Kaarakainen P, Rintala H, Vepsalainen A, Hyvarinen A, Nevalainen A, Meklin T . Microbial content of house dust samples determined with qPCR. Sci Total Environ 2009; 407: 4673–4680.

    Article  CAS  Google Scholar 

  24. Reponen T, Nevalainen A, Jantunen M, Kalliokoski P . Normal range criteria for indoor air bacteria and fungal spores in subarctic climate. Indoor Air 1992; 2: 26–31.

    Article  Google Scholar 

  25. Leppänen HK, Nevalainen A, Vepsäläinen A, Roponen M, Täubel M, Laine O et al. Determinants, reproducibility, and seasonal variation of ergosterol levels in house dust. Indoor Air 2014; 24: 248–259.

    Article  Google Scholar 

  26. Park JH, Spiegelman DL, Burge HA, Gold DR, Chew GL, Milton DK . Longitudinal study of dust and airborne endotoxin in the home. Environ Health Perspect 2000; 108: 1023–1028.

    Article  CAS  Google Scholar 

  27. Nevalainen A, Partanen P, Jaaskelainen E, Hyvarinen A, Koskinen O, Meklin T et al. Prevalence of moisture problems in Finnish houses. Indoor Air Int J Indoor Air Qual Clim 1998; 8: 45–49.

    Google Scholar 

  28. Kalatoor S, Grinshpun SA, Willeke K, Baron P . New aerosol sampler with low wind sensitivity and good filter collection uniformity. Atmos Environ 1995; 29: 1105–1112.

    Article  CAS  Google Scholar 

  29. Haugland RA, Siefring SC, Wymer LJ, Brenner KP, Dufour AP . Comparison of Enterococcus measurements in freshwater at two recreational beaches by quantitative polymerase chain reaction and membrane filter culture analysis. Water Res 2005; 39: 559–568.

    Article  CAS  Google Scholar 

  30. Haugland R, Varma M, Wymer L, Vesper S . Quantitative PCR analysis of selected Aspergillus Penicillium and Paecilomyces species. Syst Appl Microbiol 2004; 27: 198–210.

    Article  CAS  Google Scholar 

  31. Kärkkäinen PM, Valkonen M, Hyvärinen A, Nevalainen A, Rintala H . Determination of bacterial load in house dust using qPCR, chemical markers and culture. J Environ Monitor 2010; 12: 759–768.

    Article  Google Scholar 

  32. Haugland RA, Vesper SJ. Identification and Quantification of Specific Fungi and Bacteria: US Patent 6 387 652. US Patent and Trademark Office 2002. Washington, DC..

  33. Rintala H, Pitkaeranta M, Toivola M, Paulin L, Nevalainen A . Diversity and seasonal dynamics of bacterial community in indoor environment. BMC Microbiol 2008; 8.

  34. Täubel M, Rintala H, Pitkäranta M, Paulin L, Laitinen S, Pekkanen J et al. The occupant as a source of house dust bacteria. J Allergy Clin Immunol 2009; 124: 834–840.

    Article  Google Scholar 

  35. Brodie EL, DeSantis TZ, Parker JPM, Zubietta IX, Piceno YM, Andersen GL . Urban aerosols harbor diverse and dynamic bacterial populations. Proc Natl Acad Sci USA 2007; 104: 299–304.

    Article  CAS  Google Scholar 

  36. Fierer N, Liu Z, Rodriguez-Hernandez M, Knight R, Henn M, Hernandez MT . Short-term temporal variability in airborne bacterial and fungal populations. Appl Environ Microbiol 2008; 74: 200–207.

    Article  CAS  Google Scholar 

  37. 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: 713–724.

    Article  CAS  Google Scholar 

  38. Ownby DR, Peterson EL, Williams LK, Zoratti EM, Wegienka GR, Woodcroft KJ et al. Variation of dust endotoxin concentrations by location and time within homes of young children. Pediatr Allergy Immunol 2010; 21: 533–540.

    Article  Google Scholar 

  39. Hoisington AJ, Maestre JP, King MD, Siegel JA, Kinney KA . Impact of sampler selection on the characterization of the indoor microbiome via high-throughput sequencing. Build Environ 2014; 80: 274–282.

    Article  Google Scholar 

  40. Adhikari A, Kettleson EM, Vesper S, Kumar S, Popham DL, Schaffer C et al. Dustborne and airborne Gram-positive and Gram-negative bacteria in high versus low ERMI homes. Sci Total Environ 2014; 482-483: 92–99.

    Article  CAS  Google Scholar 

  41. Pitkäranta M, Meklin T, Hyvärinen 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: 233–244.

    Article  Google Scholar 

  42. 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: 236–247.

    Article  CAS  Google Scholar 

  43. Leppänen HK, Täubel M, Roponen M, Vepsäläinen A, Rantakokko P, Pekkanen J et al. Determinants, reproducibility, and seasonal variation of bacterial cell wall components and viable counts in house dust. Indoor Air 2015; 25: 260–272.

    Article  Google Scholar 

  44. Giovannangelo M, Nordling E, Gehring U, Oldenwening M, Bellander T, Heinrich J et al. Variation of biocontaminant levels within and between homes—the AIRALLERG study. J Exp Sci Environ Epidemiol 2007; 17: 134–140.

    Article  CAS  Google Scholar 

  45. Gehring U, Douwes J, Doekes G, Koch A, Bischof W, Fahlbusch B et al. Beta(1—>3)-glucan in house dust of German homes: housing characteristics, occupant behavior, and relations with endotoxins, allergens, and molds. Environ Health Perspect 2001; 109: 139–144.

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Chew GL, Rogers C, Burge HA, Muilenberg ML, Gold DR . Dustborne and airborne fungal propagules represent a different spectrum of fungi with differing relations to home characteristics. Allergy 2003; 58: 13–20.

    Article  CAS  Google Scholar 

  47. Miller JD, Laflamme AM, Sobol Y, Lafontaine P, Greenhalgh R . Fungi and fungal products in some Canadian houses. Int Biodeterioration 1988; 24: 103–120.

    Article  CAS  Google Scholar 

  48. Reponen T, Singh U, Schaffer C, Vesper S, Johansson E, Adhikari A et al. Visually observed mold and moldy odor versus quantitatively measured microbial exposure in homes. Sci Total Environ 2010; 408: 5565–5574.

    Article  CAS  Google Scholar 

  49. Barnig C, Reboux G, Roussel S, Casset A, Sohy C, Dalphin J- et al. Indoor dust and air concentrations of endotoxin in urban and rural environments. Lett Appl Microbiol 2013; 56: 161–167.

    Article  CAS  Google Scholar 

  50. Mazique D, Diette GB, Breysse PN, Matsui EC, McCormack MC, Curtin-Brosnan J et al. Predictors of airborne endotoxin concentrations in inner city homes. Environ Res 2011; 111: 614–617.

    Article  CAS  Google Scholar 

  51. Normand A, Sudre B, Vacheyrou M, Depner M, Wouters IM, Noss I et al. Airborne cultivable microflora and microbial transfer in farm buildings and rural dwellings. Occup Environ Med 2011; 68: 849–855.

    Article  Google Scholar 

  52. von Mutius E, Braun-Fahrlander C, Schierl R, Riedler J, Ehlermann S, Maisch S et al. Exposure to endotoxin or other bacterial components might protect against the development of atopy. Clin Exp Allergy 2000; 30: 1230–1234.

    Article  CAS  Google Scholar 

  53. Braun-Fahrlander C, Riedler J, Herz U, Eder W, Waser M, Grize L et al. Environmental exposure to endotoxin and its relation to asthma in school-age children. N Engl J Med 2002; 347: 869–877.

    Article  Google Scholar 

  54. van Strien RT, Engel R, Holst O, Bufe A, Eder W, Waser M et al. Microbial exposure of rural school children, as assessed by levels of N-acetyl-muramic acid in mattress dust, and its association with respiratory health. J Allergy Clin Immunol 2004; 113: 860–867.

    Article  CAS  Google Scholar 

  55. Schram D, Doekes G, Boeve M, Douwes J, Riedler J, Ublagger E et al. Bacterial and fungal components in house dust of farm children, Rudolf Steiner School children and reference children—the PARSIFAL Study. Allergy 2005; 60: 611–618.

    Article  CAS  Google Scholar 

  56. Emerson JB, Keady PB, Clements N, Morgan EE, Awerbuch J, Miller SL et al. High temporal variability in airborne bacterial diversity and abundance inside single-family residences. Indoor Air 2017; 27: 576–586.

    Article  CAS  Google Scholar 

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Acknowledgements

We thank the participating families and research analysts Katja Saarnio and Heli Martikainen for their technical assistance. The work was supported by The Finnish Work Environment Fund (grant number 115243).

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Correspondence to Hanna K Leppänen.

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Leppänen, H., Täubel, M., Jayaprakash, B. et al. Quantitative assessment of microbes from samples of indoor air and dust. J Expo Sci Environ Epidemiol 28, 231–241 (2018). https://doi.org/10.1038/jes.2017.24

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