Abstract
Children spend most of their time inside schools and bioaerosol particles are part of their everyday environment. Although bioaerosol particles are considered to be a potential risk factor for various health concerns, information concerning the indoor exposures and inhalation doses is still limited. This study aimed (i) to quantify bacterial and fungal particles levels in indoor and outdoor air of public primary schools, (ii) to assess the influence of ambient air on bacteria and fungi presence indoors, and (iii) to estimate the inhalation dose rates for respective children (8–10 years old) in comparison with adult staff. Air samples were collected in 20 primary schools in a total of 71 classrooms during heating season with a microbiological air sampler. The results showed that indoor bacterial and fungal concentrations were higher than outdoor levels (p < 0.05), which could be explained by differences in density of occupation, occupant’s activities, and inadequate ventilation. CO2 levels were significantly correlated with indoor bacteria concentrations. Moreover, mean indoor bacteria concentrations were above national limit values in all the evaluated Porto primary schools, from two to nine times higher. Regarding fungi concentrations, indoor levels were above the reference value in 75% of the schools and overall indoor levels registered a 3-fold increase compared with outdoor values. Children had two times higher inhalation dose rates to bioaerosol particles when compared to adult individuals. Thus, due to their susceptibility, special attention should be given to educational settings in order to guarantee the children healthy development.
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References
Adams RI, Miletto M, Lindow SE, Taylor JW, Bruns TD (2014) Airborne bacterial communities in residences: similarities and differences with fungi. PLoS One 9(3):e91283. https://doi.org/10.1371/journal.pone.0091283
Andersen AA (1958) New sampler for the collection, sizing, and enumeration of viable airborne particles. J Bacteriol 76:471–784
Andersen B, Frisvad JC, Sondergaard I, Rasmussen IS, Larsen LS (2011) Associations between fungal species and water-damaged building materials. Appl Environ Microbiol 77:4180–4188
Annesi-Maesano I, Baiz N, Banerjee S, Rudnai P, Rive S, Group The Sinphonie (2013) Indoor air quality and sources in schools and related health effects. J Toxicol Environ Health B 16:491–550
Bantz SK, Zhu Z, Zheng T (2014) The atopic march: progression from atopic dermatitis to allergic rhinitis and asthma. J Clin Cell Immunol 5(2):202
Barberan A, Dunn RR, Reich BJ, Pacifici K, Laber EB, Menninger HL et al (2015) The ecology of microscopic life in household dust. Proc Biol Sci 282:20151139. https://doi.org/10.1098/rspb.2015.1139
Bowers RM, McCubbin IB, Hallar AG, Fierer N (2012) Seasonal variability in airborne bacterial communities at a high-elevation site. Atmos Environ 50:41–49
Canha N, Almeida SM, do Carmo Freitas M, Wolterbeek HT. (2015). Assessment of bioaerosols in urban and rural primary schools using passive and active sampling methodologies. Archives of Environmental Protection 41:11–22
Castro D, Slezakova K, Delerue-Matos C, Alvim-Ferraz MD, Morais S, Pereira MD (2011) Polycyclic aromatic hydrocarbons in gas and particulate phases of indoor environments influenced by tobacco smoke: levels, phase distributions, and health risks. Atmos Environ 45:1799–1808
Cavaleiro-Rufo J, Madureira J, Paciência I, Aguiar L, Pereira C, Silva D, Padrão P, Moreira P, Delgado L, Annesi-Maesano I, Oliveira Fernandes E, Teixeira JP, Moreira A (2017) Indoor fungal diversity in primary schools may differently influence allergic sensitization and asthma in children. Pediatr Allergy Immunol 28(4):332–339. https://doi.org/10.1111/pai.12704
Csobod, E., Annesi-Maesano, I., Carrer, P., Kephalopoulos, S., Madureira, J., Rudnai, P., & de Oliveira Fernandes, E. (2014). Schools Indoor Pollution and Health: Observatory Network in Europe (SINPHONIE) - Final Report. The Regional Environmental Centre for Central and Eastern Europe. Italy
Dannemiller KC, Gent JF, Leaderer BP, Peccia J (2016) Influence of housing characteristics on bacterial and fungal communities in homes of asthmatic children. Indoor Air 26:179–192
Ege MJ, Mayer M, Normand A, Genuneit J, Cookson WOCM, Phil D et al (2011) Exposure to environmental microorganisms and childhood asthma. N Engl J Med 364:701–709
European Standards (2000) CSN EN 13098-Workplace atmosphere-Guidelines for measurement of airborne micro-organisms and endotoxin. Available at: http://www.en-standard.eu/csn-en-13098-workplaceatmosphere-guidelines-for-measurement-of airborne-micro-organisms-and-endotoxin
Fonseca J, Slezakova K, Morais S, Pereira MC (2014) Assessment of ultrafine particles in Portuguese preschools: levels and exposure doses. Indoor Air 24(6):618–628
Hospodsky D, Qian J, Nazaroff WW, Yamamoto N, Bibby K, Rismani-Yazdi H, et al (2012) Human Occupancy as a Source of Indoor Airborne Bacteria. PLoS ONE 7(4):e34867. https://doi.org/10.1371/journal.pone.0034867
Hospodsky D, Yamamoto N, Nazaroff WW, Miller D, Gorthala S, Peccia J (2015) Characterizing airborne fungal and bacterial concentrations and emission rates in six occupied children’s classrooms. Indoor Air 25:641–652
International Standard Organization (ISO) (2013) ISO 4833:2013—Microbiology of the food chain—Horizontal method for the enumeration of microorganisms—Part 1: Colony count at 30°C by the pour plate technique. International Organization for Standardization, Geneve
Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD et al (2012) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:1463–1464
Madureira J, Alvim-Ferraz MCM, Rodrigues S, Goncalves C, Azevedo MC, Pinto E, Mayan O (2009) Indoor air quality in schools and health symptoms among Portuguese teachers. Hum Ecol Risk Assess 15(1):159–169
Madureira J, Paciência I, Fernandes EO (2012) Levels and indoor-outdoor relationships of size-specific particulate matter in naturally ventilated Portuguese schools. J Toxicol Environ Health A 75(22–23):1423–1436
Madureira J, Pereira C, Paciência I, Teixeira JP, de Oliveira Fernandes E (2014) Identification and levels of airborne fungi in Portuguese primary schools. J Toxic Environ Health A 77(14–16):816–826. https://doi.org/10.1080/15287394.2014.909302
Madureira J, Paciência I, Rufo J, Ramos E, Barros H, Teixeira JP, de Oliveira Fernandes E (2015a) Indoor air quality in schools and its relationship with children’s respiratory symptoms. Atmos Environ 118:145–156. https://doi.org/10.1016/j.atmosenv.2015.07.028
Madureira J, Paciência I, Pereira C, Teixeira JP, de Oliveira Fernandes E (2015b) Indoor air quality in Portuguese schools: levels and sources of pollutants. Indoor Air 26:526–537. https://doi.org/10.1111/ina.12237
Madureira J, Paciência I, Rufo J, Pereira C, Teixeira JP, de Oliveira Fernandes E (2015c) Assessment and determinants of airborne bacterial and fungal concentrations in different indoor environments: homes, child day-care centers, primary schools and elderly care centers. Atmos Environ 109:139–146. https://doi.org/10.1016/j.atmosenv.2015.03.026
Meadow JF, Altrichter AE, Kembel SW, Kline J, Mhuireach G, Moriyama M, Northcutt D, O'Connor TK, Womack AM, Brown GZ, Green JL, Bohannan BJM (2014) Indoor airborne bacterial communities are influenced by ventilation, occupancy, and outdoor air source. Indoor Air 24(1):41–48. https://doi.org/10.1111/ina.12047
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
Mentese S, Arisoy M, Rad AY, Güllü G (2009) Bacteria and fungi levels in various indoor and outdoor environments in Ankara, Turkey. Clean Soil Air Water 37:487–493
Mentese S, Rad AY, Arisoy M, Gullu G (2012) Seasonal and spatial variations of bioaerosols in indoor urban environments, Ankara. Turkey. Indoor Built Environ 21:797–810
Mitchell CS, Zhang J, Sigsgaard T, Jantunen M, Lioy PJ, Samson R, Karol MH (2007) Current state of the science: health effects and indoor environmental quality. Environ Health Perspect 115:958–964
National Institute for Occupational Safety and Health (NIOSH) (1998) Bioaerosol Sampling (Indoor Air) 0800: Culturable organisms bacteria, fungi, thermophilic actinomycetes. Issue 1. NIOSH Manual of Analytical Methods (NMAM), 4th edn. NIOSH, Washington, DC
Nevalainen A (2007) Bio-aerosols as exposure agents in indoor environments in relation to asthma and allergy. In: First ENVIE Conference on Indoor Air Quality and Health for EU Policy, 2007 Helsinki, Finland
Nevalainen A, Taubel M, Hyvarinen A (2015) Indoor fungi: companions and contaminants. Indoor Air 25(2):125–126. https://doi.org/10.1111/ina.12182
Niemeier RT, Sivasubramani SK, Reponen T, Grinshpun SA (2006) Assessment of fungal contamination in moldy homes: comparison of different methods. J Occup Environ Hyg 3:262–273
Ordinance no. 353-A/ 2013 of 4th December. Republic Diary, Series I, no. 235, 4th December 2013. Ministries for Environment, Planning Territory and Energy, Health and Social Solidarity, Employment and Social Security.
Pegas PN, Alves CA, Evtyugina MG, Nunes T, Cerqueira M, Franchi M, Pio CA, Almeida SM, Verde SC, Freitas MC (2011) Seasonal evaluation of outdoor/indoor air quality in primary schools in Lisbon. J Environ Monit 13(3):657–667. https://doi.org/10.1039/c0em00472c
Qian J, Hospodsky D, Yamamoto N, Nazaroff WW, Peccia J (2012) Size-resolved emission rates of airborne bacteria and fungi in an occupied classroom. Indoor Air 22:339–351
Rintala H, Pitkaranta M, Toivola M, Paulin L, Nevalainen A (2008) Diversity and seasonal dynamics of bacterial community in indoor environment. BMC Microbiol 8:56. https://doi.org/10.1186/1471-2180-8-56
Schüepp K, and Sly PD (2012) The developing respiratory tract and its specific needs in regard to ultrafine particulate matter exposure. Paediatr Respir Rev. 13(2):95–9
US Environmental Protection Agency (2011) Exposure factors handbook. US Environmental Protection Agency, Washington, DC
Viegas C, Almeida-Silva M, Gomes AQ, Wolterbeek HT, Almeida SM (2014) Fungal contamination assessment in Portuguese elderly care centers. J Toxicol Environ Health A 77:14–23
von Mutius E (2016) The microbial environment and its influence on asthma prevention in early life. J Allergy Clin Immunol 137(3):680–689
Womack AM, Bohannan BJM, Green JL (2010) Biodiversity and biogeography of the atmosphere. PhilosTrans R Soc Lond, B, Biol Sci 365:3645–3653
World Health Organization (WHO) (2009) Dampness and Mould - WHO Guidelines for Indoor Air Quality. WHO Regional Office for Europe, Copenhagen, Denmark
Wu YH, Chan CC, Chew GL, Shih PW, Lee CT, Chao HJ (2012) Meteorological factors and ambient bacterial levels in a subtropical urban environment. Int J Biometeorol 56:1001–1009
Zhong X, Qi J, Li H, Dong L, Gao D (2016) Seasonal distribution of microbial activity in bioaerosols in the outdoor environment of the Qingdao coastal region. Atmos Environ 140:506–513
Zuraimi MS, Fang L, Tan TK, Chew FT, Tham KW (2009) Airborne fungi in low and high allergic prevalence child care centers. Atmos Environ 43:2391–2400
Funding
This study received funding from Fundação para a Ciência e a Tecnologia (FCT) through the scholarship SFRH/BPD/115112/2016 (Joana Madureira).
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Madureira, J., Aguiar, L., Pereira, C. et al. Indoor exposure to bioaerosol particles: levels and implications for inhalation dose rates in schoolchildren. Air Qual Atmos Health 11, 955–964 (2018). https://doi.org/10.1007/s11869-018-0599-8
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DOI: https://doi.org/10.1007/s11869-018-0599-8