Abstract
Fungi are one of the bioaerosols in indoor air of hospitals. They have adverse effects on staff and patients. The aim of this study was to investigate the effects of three incubation temperature on the density and composition of airborne fungi in an indoor and outdoor space of hospital. Sabouraud dextrose agar was used for culture the fungi. For improvement of aseptic properties, chloramphenicol was added to this medium. The density of airborne fungi was less than 282 CFU/m3. The highest density was detected in emergency room and the lowest of them was in neonatal intensive care unit (NICU) and operation room (OR). Results showed that fungi levels at 25 °C were higher than 37 and 15 °C (p = 0.006). In addition, ten different genera of fungi were identified in all departments. The predominant fungi were Fusarium spp., Penicillium spp., Paecilomyces spp., and Aspergillus niger. Moreover, the density and trend of distribution of Fusaruim spp. in the indoor space was directivity to outdoor space by ventilation system. The present study has provided that incubation temperature had effect on airborne fungi remarkably. We are suggested that more studies would be conducted on incubation temperature and other ambient factors on airborne fungi.
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Abbasi F, Samaei M, Khodadadi H, Karimi A, Maleknia H (2016) Effects of materials recovery facility construction on the release of fungal bioaerosols: a case study in southern Iran. Fresenius Environ Bulletin (FEB) 5:1512–1518
Al-Bader D, Alqodaiby A, Suleman P (2016) Characterization of fungi transferred by dust storms in Kuwait and their plant pathogenicity. Aerobiologia 32(2):335–345. https://doi.org/10.1007/s10453-015-9405-3
Alum A, Isaacs GZ (2016) Aerobiology of the built environment: synergy between Legionella and fungi. Am J Infect Control 44:138–143
Aquino RSS, Silveira SS, Pessoa WFB, Rodrigues A, Andrioli JL, Delabie JHC, Fontana R (2013) Filamentous fungi vectored by ants (Hymenoptera: Formicidae) in a public hospital in north-eastern Brazil. J Hosp Infect 83(3):200–204. https://doi.org/10.1016/j.jhin.2012.11.022
Arrus K, Blanka G, Abramson D, Clear R, Holley RA (2005) Aflatoxin production by Aspergillus flavus in Brazil nuts. J Stored Prod Res 41(5):513–527. https://doi.org/10.1016/j.jspr.2004.07.005
Azimi F, Naddafi K, Nabizadeh R, Hassanvand MS, Ali Mohammadi M, Afhami S, Musavi SN (2013) Fungal air quality in hospital rooms: a case study in Tehran, Iran. J Environ Health Sci Eng 11(1):30. https://doi.org/10.1186/2052-336X-11-30
Baxi SN, Portnoy JM, Larenas-Linnemann D, Phipatanakul W (2016) Exposure and health effects of fungi on humans. J Allergy Clin Immunol 4(3):396–404. https://doi.org/10.1016/j.jaip.2016.01.008
Borrego S, Perdomo (2016) Airborne microorganisms cultivable on naturally ventilated document repositories of the National Archive of Cuba. Environ Sci Pollut Res 23(4):3747–3757. https://doi.org/10.1007/s11356-015-5585-1
Cabral JPS (2010) Review) Can we use indoor fungi as bioindicators of indoor air quality? Historical perspectives and open questions. Sci Total Environ 408(20):4285–4295. https://doi.org/10.1016/j.scitotenv.2010.07.005
Greece CL, Georgiadou SP, Velegraki A, Arabatzis M, Neonakis I, Chatzipanagiotou S, Dalekos GN, Petinaki E (2014) Cluster of Fusarium verticillioides bloodstream infections among immunocompetent patients in an internal medicine department after reconstruction works. J Hosp Infect 86:267–271
Chang MW, Chung-Ru L, Hung HF, Kuo-Sheng T, Hsin H, Chun-Yu C (2014) Bioaerosols from a food waste composting plant affect human airway epithelial cell remodeling genes. Int J Environ Res Public Health 11:337–354
Choobineh AR, Rostami R, Tabatabaei SH (2008) Assessment of bioaerosols types and density in ambient air of Shiraz University of Medical Sciences Educational Hospitals. Iran Occupational Health 6(2):69–76 (Persian article)
Colls J (2002) Air pollution. Taylor & Francis Group, DOI: https://doi.org/10.4324/9780203476024
Cordeiro RA, Sn R, Brilhante R, Pantoja LD, Filho REM, Vieira PR, Rocha MF, Monteiro AJ, Sidrim JJ (2010) Isolation of pathogenic yeasts in the air from hospital environments in the city of Fortaleza, northeast Brazil. Braz J Infect Dis 14(1):30–34. https://doi.org/10.1016/S1413-8670(10)70007-6
Costa Baquiao A, Zorzete P, Alves Reis T, Assuncao E, Vergueiro S, Correa B (2012) Mycoflora and mycotoxins in field samples of Brazil nuts. Food Control 28(2):224–229. https://doi.org/10.1016/j.foodcont.2012.05.004
Darvishzadeh N, Golbabaee F, Pourmand MR, Zeini F, Rahimi Foroushani A (2013) Hospital in Tehran. Iran J Health & Environ 6 (Persian article)
Dehdashti A, Sahranavard N, Rostami R, Barkhordari A, Banaei Z (2012) Survey on density and distribution bioaerosols in indoor air of Damghan hospitals. Occupational Health Journal 4(3):41–51 (Persian article)
Douglas AP, Chen SC-A, Slavin MA (2016) Emerging infections caused by non-Aspergillus filamentous fungi. Clin Microbiol Infect 22(8):670–680. https://doi.org/10.1016/j.cmi.2016.01.011
Faridi S, Hassanvand MS, Naddafi K, Yunesian M, Nabizadeh R, Sowlat MH, Kashani H, Gholampour A, Niazi S, Zare A, Nazmara SM (2014) Indoor/outdoor relationships of bioaerosol concentrations in a retirement home and a school dormitory. Environ Sci Pollut Res 22(11):8190–8200
Fernandez-Rodriguez S, Tormo-Molina R, Maya-Manzano JM, Silva-Palacios I, Gonzalo-Garijo Á (2014) Outdoor airborne fungi captured by viable and non-viable methods. Fungal Ecol 7:16–26. https://doi.org/10.1016/j.funeco.2013.11.004
Fournel I, Sautour M, Lafon I, Sixt N, L'ollivier C, Dalle F, Chavanet P, Couillaud G, Caillot D, Astruc K, Bonnin A, Aho-Glele L-S (2010) Airborne Aspergillus contamination during hospital construction works: efficacy of protective measures. Am J Infect Control 38(3):189–194. https://doi.org/10.1016/j.ajic.2009.07.011
Freitas-Silva O, Venancio A (2011) Brazil nuts: benefits and risks associated with contamination by fungi and mycotoxins. Food Res Int 44(5):1434–1440. https://doi.org/10.1016/j.foodres.2011.02.047
Frohlich-Nowoisky J, Kampf CJ, Weber B, Huffman JA, Pohlker C, Andreae MO, Lang-Yong N, Burrows SM, Gunthe SS, Elbert W, Su H, Hoor P, Thines E, Hoffmann T, Despres VR, Poschl U (2016) Bioaerosols in the Earth system: climate, health, and ecosystem interactions. Atmos Res 182:346–376. https://doi.org/10.1016/j.atmosres.2016.07.018
Fukutomi Y, Taniguchi M (2015) Sensitization to fungal allergens: resolved and unresolved issues. Allergol Int 64(4):321–331. https://doi.org/10.1016/j.alit.2015.05.007
Gaoa M, Jiaa R, Qiua T, Hana M, Songb Y, Wang X (2015) Seasonal size distribution of airborne culturable bacteria and fungi and preliminary estimation of their deposition in human lungs during non-haze and haze days. Atmos Environ 118:203–210. https://doi.org/10.1016/j.atmosenv.2015.08.004
Georgiadou SP, Velegraki A, Arabatzis M, Neonakis I, Chatzipanagiotou S, Dalekos GN, Petinakic E (2014) Cluster of Fusarium verticillioides bloodstream infections among immunocompetent patients in an internal medicine department after reconstruction works in central Greece, Larissa. J Hosp Infect 86(4):267–271. https://doi.org/10.1016/j.jhin.2014.01.011
Gorny R, Dutkiewicz J (2002) Bacterial and fungal aerosols in indoor environment in Central and Eastern European countries. Ann Agric Environ Med 9(1):17–23
Guadalupe Marı´a LNFA-D, Duartr-Escalante EC, Marı´a D, Ezquerro C, Carmen María D, Martínez J, Acosta-Alltamirano G, Adán M, Eutimio M, Zúñiga G, García-González R, Ramírez-Pérez M, Rocío Reyes-Monte M (2016) Diversity and characterization of airborne bacteria at two health institutions. Aerobiologia 32(2):187–198. https://doi.org/10.1007/s10453-015-9389-z
Guido F, Thomas M, Regina S, Rene O, Wolfgang D (2000) Exposure to airborne fungi, MVOC and mycotoxins in biowaste-handling facilities. Int J Hyg Environ Health 203:97–104
Haleem Khan AA, Mohan Karuppayil S (2012) Fungal pollution of indoor environments and its management. Saudi J Biol Sci 19(4):405–426. https://doi.org/10.1016/j.sjbs.2012.06.002
Hedayati MT, Mayahi S, Movahedi M, Shokohi T (2011) Study on fungal flora of tap water as a potential reservoir of fungi in hospitals in Sari city, Iran. J de Mycologie Médicale / J Med Mycol 21(1):10–14. https://doi.org/10.1016/j.mycmed.2010.12.001
Hosein Zade E, Samarghandie MR, Ghiasian SA, Alikhani MY, Roshanaei G (2013) Evaluation of bioaerosols in five educational hospitals departments air in Hamedan, during 2011–2012. Joundishapour J Microbiol 6:10704 (Persian)
Hoseini M, Jabbari H, Naddafi K, Nabizadeh R, Rahbar M, Yunesian M, Jaafari J (2013) Density and distribution characteristics of airborne fungi in indoor and outdoor air of Tehran subway stations. Aerobiologia 29(3):355–363. https://doi.org/10.1007/s10453-012-9285-8
Hwang SH, Jang S, Park WM, Park JB (2016) Erratum to: Concentrations and identification of culturable airborne fungi in underground stations of the Seoul metro. Environ Sci Pollut Res 23(20):20680–20686
Ijaz MK, Zargar B, Wright KE, Rubino JR, Sattar SA (2016) Generic aspects of the airborne spread of human pathogens indoors and emerging air decontamination technologies. Am J Infect Control 44:109–120
Kim KY, Kim YS, Kim D (2010) Distribution characteristics of airborne bacteria and fungi in the general hospitals of Korea. Ind Health 48(2):236–243. https://doi.org/10.2486/indhealth.48.236
Li C, Hou P (2003) Bioaerosol characteristics in hospital clean rooms. Sci Total Environ 305(1-3):169–176. https://doi.org/10.1016/S0048-9697(02)00500-4
Ma L-J, David M, Geiser RH, Proctor AP, Rooney KOD, Frances Trail DM, Gardiner JM, Manners KK (2013) Fusarium pathogenomics. Annu Rev Microbiol 67(1):399–416. https://doi.org/10.1146/annurev-micro-092412-155650
Mandal J, Brandl H (2011) Bioaerosols in indoor environment-a review with special reference to residential and occupational locations. Environ Biol Monit J 4:83–96
Meheust D, Le Cann P, Gangneux JP (2013) Rapid quantification of viable fungi in hospital environments: analysis of air and surface samples using solid-phase cytometry. J Hosp Infect 83(2):122–126. https://doi.org/10.1016/j.jhin.2012.10.004
Naddafi K, Jabbari H, Hoseini M, Nabizadeh R, Rahbar M, Younesian M (2011) Investigation of indoor and outdoor air bacterial density in Tehran subway system. Iranian J Environ Health Sci Eng 8:383–388
Nastase I, Croitoru C, Vartirea A, Tataranu L (2016) Indoor environmental quality in operating rooms: an European standards review with regard to Romanian guidelines. Energy Procedia 85:375–382. https://doi.org/10.1016/j.egypro.2015.12.264
Niazi S, Hassanvand MS, Mahvi AH, Nabizadeh R, Alimohammadi M, Nabavi S, Faridi S, Dehghani A, Hoseini M, Moradi-Joo M, Mokamel A, Kashani H, Yarali N, Yunesian M (2015) Assessment of bioaerosol contamination (bacteria and fungi) in the largest urban wastewater treatment plant in the Middle East. Environ Sci Pollut Res Int 22(20):16014–16021. https://doi.org/10.1007/s11356-015-4793-z
Nieguitsila A, Arne P, Durand B, Deville M, Benoıt V, Chermette R, Cottenot-Latouche S, Guillot J (2011) Relative efficiencies of two air sampling methods and three culture conditions for the assessment of airborne culturable fungi in a poultry farmhouse in France. Environ Res 111(2):248–253. https://doi.org/10.1016/j.envres.2010.12.005
Noman EA, Al-Gheethi AA, Rahman NN, Nagao H, Ab Kadir MO (2016) Assessment of relevant fungal species in clinical solid wastes. Environ Sci Pollut Res Int 23(19):19806–19824. https://doi.org/10.1007/s11356-016-7161-8
Novak Babic M, Zalar P, Ženko B, Schroers H-J, Dzeroski S, Gunde-Cimerman N (2015) Candida and Fusarium species known as opportunistic human pathogens from customer-accessible parts of residential washing machines. Fungal Biol 119(2-3):95–113. https://doi.org/10.1016/j.funbio.2014.10.007
O’gorman CLM, Fuller HT (2008) Prevalence of culturable airborne spores of selected allergenic and pathogenic fungi in outdoor air. Atmospheric Environ 42(18):4355–4368. https://doi.org/10.1016/j.atmosenv.2008.01.009
Oberle M, Reichmuth M, Laffer R, Ottiger C, Fankhauser H, Bregenzer T (2015) Non-seasonal variation of airborne aspergillus spore density in a hospital building. Int J Environ Res Public Health 12(11):13730–13738. https://doi.org/10.3390/ijerph121113730
Okten S, Asan A (2012) Airborne fungi and bacteria in indoor and outdoor environment of the Pediatric Unit of Edirne Government Hospital. Environ Monit Assess 184(3):1739–1751. https://doi.org/10.1007/s10661-011-2075-x
Panagopoulou P, Filioti J, Petrikkos G, Giakouppi P, Anatoliotaki M, Farmaki E (2002) Environmental surveillance of filamentous fungi in three tertiary care hospitals in Greece. J Hosp Infect 52(3):185–191. https://doi.org/10.1053/jhin.2002.1298
Pastuszka J, Paw U, Lis D, Wlazlo A, Ulfig K (2000) Bacterial and fungal aerosol in indoor environment in Upper Silesia, Poland. Atmosphere Environ 34(22):3833–3842. https://doi.org/10.1016/S1352-2310(99)00527-0
Perdelli F, Cristina M, Spagnolo A, Dallera B, Ottria G, Grimaldi M (2006) Fungal contamination in hospital environments. Infect Control Hosp Ep 27(01):44–47. https://doi.org/10.1086/499149
Piontek M, Łuszczynska K, Lechow H (2016) Occurrence of the toxin-producing Aspergillus versicolor Tiraboschi in residential buildings. Int J Environ Res Public Health 13(9):862. https://doi.org/10.3390/ijerph13090862
Rafael T-M, Maria AG-G, Santiago F-R, Inmaculada S-P (2012) Monitoring the occurrence of indoor fungi in a hospital. Rev Iberoam Micol 29:227–234
Rainer J, Peintner U, Poder R (2001) Biodiversity and density of airborne fungi in a hospital environment. Mycopathologia 149(2):87–97. https://doi.org/10.1023/A:1007273131130
Rangaswamy BE, Fernandes F, Prakash KK, Manjunath NS (2013) Variability in airborne bacterial and fungal population in the tertiary health care centre. Aerobiologia 29(4):473–479. https://doi.org/10.1007/s10453-013-9297-z
Sanjay HC, Noel GM (2014) Review) Fungi in the cystic fibrosis lung: bystanders or pathogens? Int J Biochem Cell Biol 52:161–173
Sattar SA, Bact D (2016) Indoor air as a vehicle for human pathogens: introduction, objectives, and expectation of outcome. Am J Infect Control 44:95–101
Sautour M, Sixt N, Dalle F, Lolliver C, Calinon C, Fourquenet V (2007) Prospective survey of indoor fungal contamination in hospital during a period of building construction. J Hosp Infect 67(4):367–373. https://doi.org/10.1016/j.jhin.2007.09.013
Scheel CM, Hurst SF, Barreiros G, Akiti T, Nucci M, Balajee SA (2013) Molecular analyses of Fusarium isolates recovered from a cluster of invasive mold infections in a Brazilian hospital. BMC Infect Dis 13:49
Schomberg L, Walsh S, Tinwell B, Harrison T, Chua F (2013) Airway and parenchymal manifestations of pulmonary aspergillosis Georgia Tunnicliffe. Respir Med 107:1113–1123
Shams-Ghahfarokhi M, Aghaei-Gharehbolagh S, Aslani N, Razzaghi-Abyaneh M (2014) Investigation on distribution of airborne fungi in outdoor environment in Tehran, Iran. J Environ Health Sci Eng 12(1):54. https://doi.org/10.1186/2052-336X-12-54
Soleimani Z, Goudarzi G, Sorooshian A, Bagherian Marzounie M, Maleki H (2016) Impact of Middle Eastern dust storms on indoor and outdoor composition of bioaerosols. Atmos Environ 138:135–143. https://doi.org/10.1016/j.atmosenv.2016.05.023
Steinberg C, Laurent J, Edel-Hermann V, Barbezant M, Sixt N, Dalle F, Aho S, Bonnin A, Hartemann P, Sautour M (2015) Adaptation of Fusarium oxysporum and Fusarium dimerum to the specific aquatic environment provided by the water systems of hospitals. Water Res 76:53–65. https://doi.org/10.1016/j.watres.2015.02.036
Szyłak-Szydłowski M, Kulig A, Miaśkiewicz-Pęska E (2016) Seasonal changes in the concentrations of airborne bacteria emitted from a large wastewater treatment plant. Int Biodeterioration Biodegradation 115:11–16. https://doi.org/10.1016/j.ibiod.2016.07.008
Tanaka A, Fujiwara A, Uchida Y, Yamaguchi M, Ohta S, Homma T, Watanabe Y, Yamamoto M, Suzuki S, Yokoe T, Sagara H (2016) Evaluation of the association between sensitization to common inhalant fungi and poor asthma control. Ann Allergy Asthma Immunol 117(2):163–168. https://doi.org/10.1016/j.anai.2016.06.001
Verde SC, Almeida SM, Matos JA, Guerreiro D, Meneses M, Faria T, Botelho D, Santos M, Viegas C (2015) Microbiological assessment of indoor air quality at different hospital sites. Res Microbiol 166(7):557–563. https://doi.org/10.1016/j.resmic.2015.03.004
Vermani M, Vijayan VK, Menon B, Kausar MA, Agarwal MK (2011) Physico-chemical and clinico-immunologic studies on the allergenic significance of Aspergillus tamarii, a common airborne fungus. Immunobiology 216(3):393–401. https://doi.org/10.1016/j.imbio.2010.06.011
Wan G, Chung F, Tang C (2011) Long-term surveillance of air quality in medical center operating rooms. Ambient J. Infect Control 39(4):302–308. https://doi.org/10.1016/j.ajic.2010.07.006
Weaver L, Michels HT, Keevil CW (2010) Potential for preventing spread of fungi in air-conditioning systems constructed using copper instead of aluminium. Society for applied microbiology (sfam). Lett Appl Microbiol 50(1):18–23. https://doi.org/10.1111/j.1472-765X.2009.02753.x
Weikl F, Radl V, Munch JC, Pritsch K (2015) Targeting allergenic fungi in agricultural environments aids the identification of major sources and potential risks for human health. Sci Total Environ 529:223–230. https://doi.org/10.1016/j.scitotenv.2015.05.056
Zafar U, Nzeram P, Langarica-Fuentes A, Houlden A, Heyworth A, Saiani A, Robson GD (2014) Biodegradation of polyester polyurethane during commercial composting and analysis of associated fungal communities. Bioresour Technol 158:374–377. https://doi.org/10.1016/j.biortech.2014.02.077
Zeini F, Mehbod ASA, Emami M (2013) Comprehensive medical mycology, Teehran, University of Tehran press (Persian book)
Zhang H, Wang L, Li Z, Liu S, Xie YES, Deng X, Yang B, Liu H, Chen G, Zhao H, Zhang J (2013) A novel murine model of Fusarium solani keratitis utilizing fluorescent labeled fungi. Exp Eye Res 110:107–112. https://doi.org/10.1016/j.exer.2013.03.002
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Authors of this paper would like to express their appreciation to the personnel of hospital for their collaboration in the research process.
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This project was financially supported by Research Center for Health Sciences, Shiraz University of Medical Sciences (No. 92-01-42-7118).
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Abbasi, F., Samaei, M. The effect of temperature on airborne filamentous fungi in the indoor and outdoor space of a hospital. Environ Sci Pollut Res 26, 16868–16876 (2019). https://doi.org/10.1007/s11356-017-0939-5
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DOI: https://doi.org/10.1007/s11356-017-0939-5