Abstract
This study aimed at determining culturable airborne bacteria (CAB) and fungi (CAF) concentrations in different sections of a primary school located in Istanbul. Occupancy variables were determinants of exposure and the environmental, ventilation, and comfort parameters within the study. Air samples were collected twice in the summer and spring seasons using a microbial air sampler (Sampl’air™) and were analyzed in terms of CAB and CAF concentrations. Obtained results were visualized using geographic information system (GIS) technology for presenting the spatial variations of CAB and CAF concentrations with respect to environmental determinants and changing weather conditions as temperature and humidity. The study introduced that the CAB and CAF concentrations vary indoors based on the sampling location and human occupancy. As an interesting finding of the study, CAB (3300 CFU/m3) and CAF (3100 CFU/m3) concentrations in the 5th classroom, where relative humidity and temperature values were recorded as 62% and 25.3 °C, respectively, were observed, confirming higher values than those of communal areas. This result proved the importance of indoor characteristics like location, ventilation, occupation time, and hygiene as the substantial determinants of CAB and CAF exposure besides the indoor population. This study emphasized the importance of regular and systematic monitoring of airborne microorganisms in different sections of schools using objective and quantitative methodologies in terms of providing healthy educational environments for students.
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References
Ali MY, Hanafiah MM, Latif MT (2016) Composition and distribution of particulate matter (PM10) in a mechanically ventilated university building. In AIP Conference Proceedings, 1784 (1) AIP Publishing, p 060017. https://doi.org/10.1063/1.4966855
Aliabadi AA, Rogak SN, Bartlett KH, Green SI (2011) Preventing airborne disease transmission: review of methods for ventilation design in health care facilities. Adv Prev Med 2011(124064):21. https://doi.org/10.4061/2011/124064
Alkoy S, Dogru AO, Basaraner M, Sahin U, Ulugtekin N, Seker DZ (2009) Determination of the epidemiological aspects of air pollution in Istanbul by utilizing GIS. Fresenius Environ Bull 18(1):117–122
Asan A, Özkale E, Kalyoncu F (2016) Checklist of Cladosporium species reported from Turkey. CBU J Sci 12:221–229. https://doi.org/10.18466/cbujos.47932
Bıçakçı A, Tatlıdil S, Canıtez Y, Malyer H, Sapan N (2001) Allergen Alternaria sp. and Cladosporium sp. spores in the atmosphere of Mustafakemalpaşa (Bursa). Turkiye Klinikleri Arch Lung 2:69–72 (Article in Turkish)
Burge HA (2000) The Fungi. In: Spengler JD, Jonathan MS, McCarthy JF (eds) Indoor Air Quality Handbook. McGraw-Hill Companies, Inc., New York
Bush RK, Portnoy JM, Saxon A, Terr AI, Wood RA (2006) The medical effects of mold exposure. J Allergy Clin Immunol 117:326–333. https://doi.org/10.1016/j.jaci.2005.12.001
Çetinkaya Z, Fidan F, Ünlü M, Hasenekoğlu İ, Tetik L, Demirel R (2005) Allergic fungal spores in the atmosphere of Afyon city. Turkiye Klinikleri Arch Lung 6:140–144 (Article in Turkish)
Chang CW, Chung H, Huang CFH, Su J (2001) Exposure of workers to airborne microorganisms in open-air swine house. Appl Environ Microbiol 67:155–161. https://doi.org/10.1128/AEM.67.1.155-161.2001
Chang FY, Lee JH, Yang YH, Yu HH, Wang LC, Lin YT, Chiang BL (2011) Analysis of the serum levels of fungi-specific immunoglobulin E in patients with allergic diseases. Int Arch Allergy Immunol 154:49–56. https://doi.org/10.1159/000319208
Chang CW, Ting YT, Horng YJ (2019) Collection efficiency of liquid-based samplers for fungi in indoor air. Indoor Air 29:380–389. https://doi.org/10.1111/ina.12535
Clauß M, Springorum AC, Schulz J, Hartung J (2012) High temporal resolution measurements of mould spores and bacteria in ambient air-influence of fluctuations on the results of different sampling methods for the detection of natural background concentrations. Gefahrst Reinhalt Luft 72:155–161
Çobanoğlu N, Kiper N (2006) Potential threat of inhalation indoor air in buildings. Journal of Children’s Health and Diseases. Cocuk Sagligi Hast Derg 49:71–75
Çobanoğlu N, Pekcan S, Aslan A, Kiper N (2005) Outdoor and indoor air pollution. Asthma Allergy Immunol 3(1):77–85
Denning DW, O'Driscoll BR, Hogaboam CM, Bowyer P, Niven RM (2006) The link between fungi and severe asthma: a summary of the evidence. Eur Respir J 27:615–626. https://doi.org/10.1183/09031936.06.00074705
Dharan S, Pittet D (2002) Environmental controls in operating theatres. J Hosp Infect 51:79–84. https://doi.org/10.1053/jhin.2002.1217
Dillon HK, Miller JD, Sorenson WG, Douwes J, Jacobs RR (1999) Review of methods applicable to the assessment of mold exposure to children. Environ Health Perspect 107:473–480. https://doi.org/10.1289/ehp.99107s3473
Dogru AO, David RM, Ulugtekin N, Goksel C, Seker DZ, Sözen S (2017) GIS based spatial pattern analysis: children with hepatitis A in Turkey. Environ Res 156:349–357. https://doi.org/10.1016/j.envres.2017.04.001
Ege MJ, Mayer M, Normand A, Genuneit J, Cookson WOCM, Phil D, Braun-Fahrlander C, Heedrik D, Piarroux R, von Mutius E (2011) Exposure to environmental microorganisms and childhood asthma. N Engl J Med 364:701–709. https://doi.org/10.1056/NEJMoa1007302
Environment Protection Agency (EPA) (2003) Indoor air quality tools for schools: IAQ coordinator’s guide. US Environmental Protection Agency, pp 1–78, U.S. Government Printing Office, Washington, DC. Accessed on 30 October 2019 https://www.epa.gov/iaq-schools/indoor-air-quality-tools-schools-action-kit
Eugster S, Schawalder P, Gaschen F, Boerlin P (2004) A prospective study of postoperative surgical site infections in dogs and cats. Vet Surg 33:542–550. https://doi.org/10.1111/j.1532-950X.2004.04076.x
Fan XJ, Yang C, Zhang L, Fan Q, Li T, Bai X, Zhao Z, Zhang X, Norback D (2017) Asthma symptoms among Chinese children: the role of ventilation and PM10 exposure at school and home. Int J Tuberc Lung Dis 21(11). https://doi.org/10.5588/ijtld.17.0196
Farzana D (2013) Application of GIS in visualization and assessment of ambient air quality for SO2 in Lima Ohio, Theses and Dissertations,The University of Toledo, 56
Fromme H, Twardella D, Dietrich S, Heitmann D, Schierl R, Liebl B, Rüden H (2007) Particulate matter in the indoor air of classrooms—exploratory results from Munich and surrounding area. Atmos Environ 41:854–866. https://doi.org/10.1016/j.atmosenv.2006.08.053
Galante D, Hartung De Capriles C, Mata-Essayag S, Conesa A, Córdova Y, Trejo E, Tassinari P (2006) Respiratory allergies in Venezuela: are fungi responsible? Mycoses 49:493–498. https://doi.org/10.1111/j.1439-0507.2006.01273.x
Garrett MH, Rayment PR, Hooper MA, Abramson MJ, Hooper BM (1998) Indoor airborne fungal spores, house dampness and associations with environmental factors and respiratory health in children. Clin Exp Allergy 28:459–467. https://doi.org/10.1046/j.1365-2222.1998.00255.x
Godish DR, Godish TJ (2007) Relationship between sampling duration and concentration of culturable airborne mould and bacteria on selected culture media. J Appl Microbiol 102:1479–1484. https://doi.org/10.1111/j.1365-2672.2006.03200.x
Greenacre M, Primicerio R (2013) Multivariate analysis of ecological data. Fundacio BBVA. Accessed 2 April 2019. https://www.fbbva.es/wp-content/uploads/2017/05/dat/DE_2013_multivariate.pdf. Accessed 2 April 2019.
Hargreaves M, Parappukkaran S, Morawska L, Hitchins J, He C, Gilbert D (2003) A pilot investigation into association between indoor airborne fungal and non-biological particle concentrations in residential houses in Brisbane, Australia. Sci Total Environ 312:89–101. https://doi.org/10.1016/S0048-9697(03)00169-4
Hosokawa R, Katsura T (2018) Association between mobile technology use and child adjustment in early elementary school age. PLoS One 13:e0208844. https://doi.org/10.1371/journal.pone.0199959
Idris SAA, Hanafiah MM, Ismail M, Abdullah S, Khan MF (2020) Laboratory air quality and microbiological contamination in a university building. Arab J Geosci 13:580. https://doi.org/10.1007/s12517-020-05564-8
Jones AM, Harrison RM (2004) The effects of meteorological factors on atmospheric bioaerosol concentrations–a review. Sci Total Environ 326:151–180. https://doi.org/10.1016/j.scitotenv.2003.11.021
Kim KH, Kabir H, Jahan SA (2018) Airborne bioaerosols and their impact on human health. J Environ Sci 67:23–35. https://doi.org/10.1016/j.jes.2017.08.027
Korsavi SS, Montazami A, Mumovic D (2020) Indoor air quality (IAQ) in naturally-ventilated primary schools in the UK: occupant-related factors. Build Environ 180:106992. https://doi.org/10.1016/j.buildenv.2020.106992
Lacey J, Crook B (1988) Fungal and actinomycete spores as pollutants of the workplace and occupational allergens. Ann Occup Hyg 32:515–533. https://doi.org/10.1093/annhyg/32.4.515
Larsen L, Gravesen S (1991) Seasonal variation of outdoor airborne viable microfungi in Copenhagen, Denmark. Grana 30:467–471. https://doi.org/10.1080/00173139109432011
Laumbach R, Meng QY, Kipen H (2015) What can individuals do to reduce personal health risks from air pollution? J Thorac Dis 7:96–107. https://doi.org/10.3978/j.issn.2072-1439.2014.12.21
Liang R, Xiao P, She R, Han S, Chang L, Zheng L (2013) Culturable airborne bacteria in outdoor poultry-slaughtering facility. Microbes Environ 28:251–256. https://doi.org/10.1264/jsme2.ME12178
Lin WH, Li CS (2000) Associations of fungal aerosols, air pollutants, and meteorological factors. Aerosol Sci Technol 32:359–368. https://doi.org/10.1080/027868200303678
Mandal J, Brandl H (2011) Bioaerosols in indoor environment - a review with special reference to residential and occupational locations. Open Environ Biol Monit J 4:83–96. https://doi.org/10.2174/1875040001104010083
Meng QY, Spector D, Colome S, Turpin B (2009) Determinants of indoor and personal exposure to PM (2.5) of indoor and outdoor origin during the RIOPA study. Atmos Environ 43:5750–5758. https://doi.org/10.1016/j.atmosenv.2009.07.066
Mi YH, Norbäck D, Tao J, Mi YL, Ferm M (2006) Current asthma and respiratory symptoms among pupils in Shanghai, China: influence of building ventilation, nitrogen dioxide, ozone, and formaldehyde in classrooms. Indoor Air 16:454–464. https://doi.org/10.1111/j.1600-0668.2006.00439.x
Miller MR, Newby DE (2020) Air pollution and cardiovascular disease: car sick. Cardiovasc Res 116:279–294. https://doi.org/10.1093/cvr/cvz228
Miller JD, Haisley PD, Reinhardt JH (2000) Air sampling results in relation to the extent of fungal colonization of building materials in some water-damaged buildings. Indoor Air 10:146–151
Ministry of Environment, Republic of Korea (2019) www.me.go.kr, Accessed on 30 October 2019. http://eng.me.go.kr/eng/web/index.do?menuId=468
Morawska L (2005), Droplet Fate in Indoor Environments, or Can We Prevent the Spread of Infection? In: Yang X, Zhao B, Zhao, R (ed) Indoor Air 2005: Proceedings of the 10th International Conference on Indoor Air Quality and Climate. Tsinghua University Press, CD Rom, pp. 9-23.
Muilenberg M (1995) The outdoor aerosol. In: Burge HA (ed) Bioaerosols, 1st edn. Lewis. CRC Press, Boca Raton, pp 163-204
Mutlu T (2016) Understanding students’ and teachers’ approaches to tablet use in Turkish secondary schools: a model based approach, PhD dissertation, The University of Sheffield School of Education
Nazaroff WW (2016) Indoor bioaerosol dynamics. Indoor Air 26:61–78. https://doi.org/10.1111/ina.12174
Rolandi L, Lodola L, Guglielminetti M, Caretta G, Azzaretti G (1998) Evaluation of airborne particulate and fungi in critical hospital care units. Toxicol Lett 95(1):226
Saxena G, Mittal N, Mukerji KG, Arora DK (1991) Nematophagous fungi in the biological control of nematodes. In: Arora DK, Ajello L, Mukerji KG (eds) Handbook of applied mycology. Marcel Dekker Inc, New York, pp 707–733
Sivri N, Bağcigil AF, Metiner K, Şeker DZ, Orak S, Güneş Durak S, Sönmez VZ (2016) Culturable airborne bacteria and isolation of methicillin-resistant coagulase-negative staphylococci from outdoor environments on European side of Istanbul, Turkey. Arch Environ Prot 42:77–86. https://doi.org/10.1515/aep-2016-0034
Sun Y, Wang Z, Zhang Y, Sundell J (2011) In China, students in crowded dormitories with a low ventilation rate have more common colds: evidence for airborne transmission. PLoS One 6(11):e27140. https://doi.org/10.1371/journal.pone.0027140
Tatlıdil S, Bıçakçı A, Akkaya A, Malyer H (2001) Allergen Cladosporium sp. and Alternaria sp. spores in the atmosphere of Burdur. Med J SDU 8:1–3
Thomas S, Palmer R, Phillipo E, Chipungu G (2016) Reducing bacterial contamination in an orthopedic theatre ventilated by natural ventilation, in a developing country. J Infect Dev Ctries 10:518–522. https://doi.org/10.3855/jidc.7436
URL 1. ISO/FDIS14698-1(2003) Cleanrooms and associated controlled environments – biocontamination control – part 1: general principles and methods General principles and methods. https://www.iso.org/obp/ui/#iso:std:iso:14698:-1:ed-1:v1:en Accessed 2 November 2020
URL 2. Sampl’airTM Brochure (2018) Accessed 2 November 2020 https://www.biomerieux-usa.com/sites/subsidiary_us/files/samplair_broc.pdf
Walser SM, Gerstner DG, Brenner B, Bünger J, Eikmann T, Janssen B, Kolb S, Kolk A, Nowak D, Raulf M, Sagunski H, Sedlmaier N, Suchenwirth R, Wiesmüller G, Wollin KM, Tesseraux I, Herr CE (2015) Evaluation of exposure-response relationships for health effects of microbial bioaerosols - a systematic review. Int J Hyg Environ Health 218:577–589. https://doi.org/10.1016/j.ijheh.2015.07.004
Wanner H-U, Gravesen S (1993) Biological particles in indoor environments: European Collaborative Action. Indoor Air Quality & Its Impact on Man. Report No. 12. Luxembourg: Commission of the European Communities, Directorate General for Science, Research and Development. Joint Research Institute - Environment Institute
World Health Organization (WHO) (1988) Indoor air quality: biological contaminants. World Health Organization, European Series, n. 31, Copenhagen, Denmark
Zhang X, Zhao Z, Nordquist T, Norback D (2011) The prevalence and incidence of sick building syndrome in Chinese pupils in relation to the school environment: a two-year follow-up study. Indoor Air 21:462–471. https://doi.org/10.1111/j.1600-0668.2011.00726.x
Acknowledgments
The authors kindly thank Erçağ Önen, the principal of the primary school where the case study was performed, for his valuable support and contributions during field measurements. Additionally, Dr. M. Kutay Sivri is greatly acknowledged for his opinions and suggestions which contributed to the writing progress of this manuscript.
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Sivri, N., Dogru, A.O., Bagcigil, A.F. et al. Assessment of the indoor air quality based on airborne bacteria and fungi measurements in a public school of Istanbul. Arab J Geosci 13, 1291 (2020). https://doi.org/10.1007/s12517-020-06252-3
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DOI: https://doi.org/10.1007/s12517-020-06252-3