Skip to main content

Advertisement

SpringerLink
Log in

Indoor airborne fungal pollution in newborn units in Turkey

  • Published:
Environmental Monitoring and Assessment Aims and scope Submit manuscript

Abstract

Pathogenic and/or opportunistic fungal species are major causes of nosocomial infections, especially in controlled environments where immunocompromised patients are hospitalized. Indoor fungal contamination in hospital air is associated with a wide range of adverse health effects. Regular determination of fungal spore counts in controlled hospital environments may help reduce the risk of fungal infections. Because infants have inchoate immune systems, they are given immunocompromised patient status. The aim of the present study was to evaluate culturable airborne fungi in the air of hospital newborn units in the Thrace, Marmara, Aegean, and Central Anatolia regions of Turkey. A total of 108 air samples were collected seasonally from newborn units in July 2012, October 2012, January 2013, and April 2013 by using an air sampler and dichloran 18% glycerol agar (DG18) as isolation media. We obtained 2593 fungal colonies comprising 370 fungal isolates representing 109 species of 28 genera, which were identified through multi-loci gene sequencing. Penicillium, Aspergillus, Cladosporium, Talaromyces, and Alternaria were the most abundant genera identified (35.14, 25.40, 17.57, 2.70, and 6.22% of the total, respectively).

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Alangaden, G. J. (2011). Nosocomial fungal infections: epidemiology, infection control, and prevention. Infectious Disease Clinics of North America, 25(1), 201–225.

    Article  Google Scholar 

  • Araujo, R., & Cabral, J. P. (2010). Fungal air quality in medical protected environments. pp. 357–382 (chapter 17). In A. Kumar (Ed.), Air quality. Rijeka: InTech Open Access Publisher.

  • Andersen, A. A. (1958). New sampler for the collection, sizing and enumeration of viable airborne particles. Journal of Bacteriology, 76(5), 471–484.

    CAS  Google Scholar 

  • Awad, A. H. A. (2005). Vegetation: a source of air fungal bio-contaminant. Aerobiologia, 21(1), 53–61.

    Article  Google Scholar 

  • Barbosa, J., Vieira, R., Costa, J., Moreira, L., Fernandes, A., Madeira, C., et al. (2012). Prevalence of Aspergillus sp. in Portuguese Infant and Elementary Schools. Air Water Borne Diseases, 1(2), 1–3.

    Google Scholar 

  • Bogomolova, E., & Kirtsideli, I. (2009). Airborne fungi in four stations of the St. Petersburg Underground railway system. International Biodeterioration and Biodegradation, 63(2), 156–160.

    Article  CAS  Google Scholar 

  • Caggiano, G., Napoli, C., Coretti, C., Lovero, G., Scarafile, G., De Giglio, O., et al. (2014). Mold contamination in a controlled hospital environment: a 3-year surveillance in southern Italy. BMC Infectious Diseases, 14, 595.

    Article  Google Scholar 

  • Carbone, I., & Kohn, L. M. (1999). A method for designing primer sets for speciation studies in filamentous ascomycetes. Mycologia, 91(3), 553–556.

    Article  CAS  Google Scholar 

  • Choi, Y. W., Hyde, K. D., & Ho, W. H. (1999). Single spore isolation of fungi. Fungal Diversity, 3, 29–38.

    Google Scholar 

  • Çetinkaya, Z., Fidan, F., Ünlü, M., Hasenekoğlu, İ., Tetik, L., & Demirel, L. (2005). The allergic fungal spores in the atmosphere of Afyon City. Turkiye Klinikleri Archives of Lung, 6(4), 140–144.

    Google Scholar 

  • Dagenais, T. R. T., & Keller, N. P. (2009). Pathogenesis of Aspergillus fumigatus in invasive aspergillosis. Clinical Microbiology Reviews, 22(3), 447–465.

    Article  CAS  Google Scholar 

  • Demirel, R., & Sariozlu, N. Y. (2014). Mycotoxigenic moulds and mycotoxins in flours consumed in Turkey. Journal of the Science of Food and Agriculture, 94(8), 1577–1584.

    Article  CAS  Google Scholar 

  • Desoubeaux, G., Bernard, M. C., Gros, V., Sarradin, P., Perrodeau, E., Vecellio, L., et al. (2014). Testing an innovative device against airborne Aspergillus contamination. Medical Mycology, 52(6), 584–590.

    Article  Google Scholar 

  • Dessi, A. (2014). Neonatal fungal infections: new strategies in diagnosis. Journal of Pediatric and Neonatal Individualized Medicine, 3(2), e030222.

    Google Scholar 

  • Ellsworth, M., Sims, C. R., & Osrosky-Zeichner, L. (2012). Neonatal fungal infections (chapter 17). In R. K. Ohls & A. Maheshwari (Eds.), Hematology, immunology and infectious disease: neonatology questions and controversies (2nd ed., pp. 287–302). Philadelphia: PA Elsevier/Saunders.

    Chapter  Google Scholar 

  • EL-Morsy, E. S. M. (2006). Preliminary survey of indoor and outdoor airborne microfungi at coastal buildings in Egypt. Aerobiologia, 22(3), 197–210.

    Article  Google Scholar 

  • Fang, Z., Tang, Q., Gong, C., Ouyang, Z., Liu, P., Sun, L., et al. (2015). Profile and distribution characteristics of culturable airborne fungi in residential homes with children in Beijing, China. Indoor and Built Environment, 0(0), 1–11.

    Google Scholar 

  • Gangneux, J. P., Robert-Gangneux, F., Gicquel, G., Tanquerel, J. J., Chevrier, S., Poisson, M., et al. (2006). Bacterial and fungal counts in hospital air: comparative yields for 4 sieve impactor air samplers with 2 culture media. Infection Control and Hospital Epidemiology, 27(12), 1405–1408.

    Article  Google Scholar 

  • Garnacho-Montereo, J., & Amaya-Villar, R. (2006). A validated clinical approach for the management of aspergillosis in critically ill patients: ready, steady, go! Critical Care, 10(2), 132.

    Article  Google Scholar 

  • Halem Khan, A. A., & Mohan Karuppayil, S. (2012). Fungal pollution of indoor environments and its management. Saudi Journal of Biological Sciences, 19(4), 405–426.

    Article  Google Scholar 

  • Hundalani, S., & Pammi, M. (2013). Invasive fungal infections in newborns and current management strategies. Expert Review of Anti-Infective Therapy, 11(7), 709–721.

    Article  CAS  Google Scholar 

  • Jung, C. C., Wu, P. C., Tseng, C. H., & Su, H. J. (2015). Indoor air quality varies with ventilation types and working areas in hospitals. Building and Environment, 85, 190–195.

    Article  Google Scholar 

  • Kalkanci, A., Kustimur, S., Sucak, G. T., Senol, E., Sugita, T., Adams, G., Verkley, G., & Summerbell, R. (2006). Fulminating fungal sinusitis caused by Valsa sordida, a plant pathogen, in a patient immunocompromised by acute myeloid leukemia. Medical Mycology, 44(6), 531–539.

    Article  CAS  Google Scholar 

  • Karalti, I., & Colakoglu, G. (2012). The seasonal distribution of airborne fungi in two hospitals in Istanbul. African Journal of Biotechnology, 11(44), 10272–10279.

    Google Scholar 

  • Kocazeybek, B., Ordu, A., Ayyıldız, A., Aslan, M., Sönmez, B., & Demiroğlu, C. (2000). The investigation of the different methods for measuring air cleanliness of operation rooms in surgical centres: a study with three centres. Hastane Infeksiyonlari Dergisi, 4(3), 164–170.

    Google Scholar 

  • Lymperopoulou, D. S., Adams, R. I., & Lindow, S. E. (2016). Contribution of vegetation to the microbial composition of nearby outdoor air. Applied and Environmental Microbiology, 82(13), 3822–3833.

    Article  CAS  Google Scholar 

  • Manzoni, P., Rizzollo, S., Monetti, C., Carbonara, C., Priolo, C., Mastretta, E., et al. (2012). Neonatal cutaneous disseminated aspergillosis in a preterm extremely-low-birth-weight infant with favourable outcome at 3-year follow-up: a case report. Early Human Development, 88(2), S65–S68.

    Article  Google Scholar 

  • Méheust, D., Le Cann, P., & Gangneux, J. P. (2013). Rapid quantification of viable fungi in hospital environments: analysis of air and surface samples using solid-phase cytometry. Journal of Hospital Infection, 83(2), 122–126.

    Article  Google Scholar 

  • Méheust, D., Le Cann, P., Reboux, G., Millon, L., & Gangneux, J. P. (2014). Indoor fungal contamination: health risks and measurement methods in hospitals, homes and workplaces. Critical Reviews in Microbiology, 40(3), 248–260.

    Article  Google Scholar 

  • Montagna, M. T., Lovero, G., De Giglio, O., Latta, R., Caggiano, G., Montagna, O., et al. (2010). Invasive fungal infections in neonatal intensive care units of Southern Italy: a multicentre regional active surveillance (AURORA Project). Journal of Preventive Medicine and Hygiene, 51(3), 125–130.

    CAS  Google Scholar 

  • Munoz, P. A., & Bouza, E. (2001). Environmental surveillance and other control measures in the prevention of nosocomial fungal infections. Clinical Microbiology and Infection, 7(2), 38–45.

    Article  Google Scholar 

  • Okten, S., & Asan, A. (2012). Airborne fungi and bacteria in indoor and outdoor environment of the Pediatric Unit of Edirne Government Hospital. Environmental Monitoring and Assessment, 184(3), 1739–1751.

    Article  Google Scholar 

  • Perlroth, J., Choi, B., & Spellberg, B. (2007). Nosocomial fungal infections: epidemiology, diagnosis, and treatment. Medical Mycology, 45(4), 321–346.

    Article  Google Scholar 

  • Rainer, J., Peintner, U., & Poder, R. (2000). Biodiversity and concentration of airborne fungi in a hospital environment. Mycopathologia, 149(2), 87–97.

    Article  Google Scholar 

  • Rao, C. Y., Burge, H. A., & Chang, J. C. S. (1996). Review of quantitative standards and guidelines for fungi in indoor air. Journal of the Air., & Waste Management Association, 46(9), 899–908.

    Article  CAS  Google Scholar 

  • Rao, S., & Ali, U. (2005). Systemic fungal infections in neonates. Journal of Postgraduate Medicine, 51(1), S27–S29.

    Google Scholar 

  • Rippon, J. W., Gerhold, R., & Heath, M. (1980). Thermophillic and thermotolerant fungi isolated from the thermal effluent of nuclear power generating reactors: dispersal of human opportunistic and veterinary pathogenic fungi. Mycopathologia, 70(3), 169–179.

    Article  CAS  Google Scholar 

  • Ross, C., Menezes, J. R., Svidzinski, T. I. E., Albino, U., & Andrade, G. (2004). Studies on fungal and bacterial population of air conditioned environments. Brazilian Archives of Biology and Technology., 47(5), 827–835.

    Article  Google Scholar 

  • Rowen, J. L. (2001). Fungal infections in the neonatal intensive care unit. Seminars in Pediatric Infectious Diseases, 12(4), 107–114.

    Article  Google Scholar 

  • Samson, R. A., Houbraken, J., Thrane, U., Frisvad, J. C., & Andersen, B. (2010). Food and indoor fungi. 390 pp. Utrecht: CBS KNAW Fungal Diversity Centre.

    Google Scholar 

  • Samson, R. A., Seifert, K. A., Kuijpers, A. F. A., Houbraken, J., & Frisvad, J. C. (2004). Phylogenetic analysis of Penicillium subgenus Penicillium using partial beta-tubulin sequences. Studies in Mycology, 49, 175–200.

    Google Scholar 

  • Samson, R. A., Visagie, C. M., Houbraken, J., Hong, S. B., Hubka, V., Klaassen, C. H. W., et al. (2014). Phylogeny, identification and nomenclature of the genus Aspergillus. Studies in Mycology, 78, 141–173.

    Article  CAS  Google Scholar 

  • Saracli, M. A., Mutlu, F. M., Yildiran, S. T., Kurekci, A. E., Gonlum, A., Uysal, Y., et al. (2007). Clustering of invasive Aspergillus ustus eye infections in a tertiary care hospital: a molecular epidemiologic study of an uncommon species. Medical Mycology, 45(4), 377–384.

    Article  CAS  Google Scholar 

  • Sarica, S., Asan, A., Tatman-Otkun, M., & Ture, M. (2002). Monitoring indoor airborne fungi and bacteria in the different areas of Trakya University Hospital (Edirne-Turkey). Indoor and Built Environment, 11(5), 285–292.

    Article  Google Scholar 

  • Serra, R., Cabañes, F.J., Perrone, G., Castella, G., Venancio, A., Mule, G., et al. (2006). Aspergillus ibericus: a new species of section Nigri isolated from grapes. Mycologia, 98(2), 295–306.

  • Shoham, S., & Marwaha, S. (2010). Invasive fungal infections in the ICU. Journal of Intensive Care Medicine, 25(2), 78–92.

    Article  Google Scholar 

  • Singh, N., & Paterson, D. L. (2005). Aspergillus infections in transplant recipients. Clinical Microbiology Reviews, 18(1), 44–69.

    Article  CAS  Google Scholar 

  • Srinivasan, A., Beck, C., Buckley, T., Geyh, A., Bova, G., Merz, W., et al. (2002). The ability of hospital ventilation systems to filter Aspergillus and other fungi following a building implosion. Infection Control., & Hospital Epidemiology, 23(9), 520–524.

    Article  Google Scholar 

  • Tamura, K., Stecher, G., Peterson, D., Filipski, A., & Kumar, S. (2013). MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution, 30(12), 2725–2729.

    Article  CAS  Google Scholar 

  • Topbas, M., Tosun, I., Çan, G., Kaklikkaya, N., & Aydin, F. (2006). Identification and seasonal distribution of airborne fungi in urban outdoor air in an Eastern Black Sea Turkish Town. Turkish Journal of Medical Sciences, 36(1), 31–36.

    Google Scholar 

  • Uztan, A. H., Ates, M., Gunyar, O. A., Gulbahar, O., Baydal, B., & Boyacioglu, H. (2013). Airborne microfungus flora determined in the different units of the department of internal diseases, Ege University Hospital. Fresenius Environmental Bulletin, 22(11), 3251–3257.

    Google Scholar 

  • Vackova, M., Buchta, V., Prymula, R., Cerman, J., Kubatova, A., Hamal, P., et al. (2006). The occurrence of microscopic fungi in air samples from a transplant intensive care unit. Indoor and Built Environment, 15(1), 115–118.

    Article  Google Scholar 

  • Visagie, C. M., Houbraken, J., Frisvad, J. C., Hong, S. B., Klaassen, C. H. W., Perrone, G., et al. (2014). Identification and nomenclature of the genus Penicillium. Studies in Mycology, 78, 343–371.

    Article  CAS  Google Scholar 

  • W.H.O. (2009). Who guidelines for indoor air quality: dampness and mould. Copenhagen: WHO Regional Office for Europe.

  • Wu, P. C., Su, H. J., & Ho, H. M. (2000). A comparison of sampling media for environmental viable fungi collected in a hospital environment. Environmental Research, 82(3), 253–257.

    Article  CAS  Google Scholar 

  • Yamamoto, N., Bibby, K., Qian, J., Hospodsky, D., Rismani-Yazdi, H., Nazaroff, W. W., & Peccia, J. (2012). Particle-size distributions and seasonal diversity of allergenic and pathogenic fungi in outdoor air. The ISME Journal, 6(10), 1801–1811.

    Article  CAS  Google Scholar 

  • Zorman, T., & Jersek, B. (2008). Assessment of bioaerosol concentrations in different indoor environments. Indoor and Built Environment, 17(2), 155–163.

    Article  Google Scholar 

Download references

Acknowledgements

We are very grateful to the “The Scientific and Technological Research Council of Turkey-TUBITAK” for financially supporting our study, Project Number: 111T925. Also special thanks to the Management of CBS-KNAW Fungal Biodiversity Centre (Utrecht-The Netherlands) and Prof. Dr. Robert A. SAMSON for their support in molecular studies in their laboratory for some problematic fungal species from our project and for their kind permission for some of our project staff for working there for certain periods. We wish to thanks Neonatal Managers of Trakya University Medical Faculty, Istanbul University Istanbul Medical Faculty, Eskisehir Osmangazi University Medical Faculty, Ege University Medical Faculty, and Celal Bayar University Medical Faculty for allow our study in mentioned units.

Author information

Authors and Affiliations

  1. Faculty of Science Department of Biology, Anadolu University, 26470, Eskisehir, Turkey

    Rasime Demirel, Derya Berikten & Merih Kivanc

  2. Faculty of Science Department of Biology, Trakya University, Edirne, Turkey

    Burhan Sen, Suzan Okten, Halide Aydogdu, Ahmet Asan & Soner Ozdil

  3. Faculty of Science Department of Biology, Istanbul University, Istanbul, Turkey

    Duygu Kadaifciler

  4. Faculty of Science Department of Biology, Ege University, Izmir, Turkey

    Aysegul Yoltas, Alev Haliki Uztan, Ozlem Abaci Gunyar & Erhan Sakartepe

  5. Faculty of Science and Art Department of Biology, Celal Bayar University, Manisa, Turkey

    Evrim Ozkale

  6. Westerdijk Fungal Biodiversity Institute, Utrecht, The Netherlands

    Robert A. Samson & Neriman Yilmaz

Authors
  1. Rasime Demirel
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Burhan Sen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Duygu Kadaifciler
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Aysegul Yoltas
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Suzan Okten
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Evrim Ozkale
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Derya Berikten
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Robert A. Samson
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Alev Haliki Uztan
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Neriman Yilmaz
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Ozlem Abaci Gunyar
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Halide Aydogdu
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Ahmet Asan
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Merih Kivanc
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Soner Ozdil
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Erhan Sakartepe
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rasime Demirel.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Demirel, R., Sen, B., Kadaifciler, D. et al. Indoor airborne fungal pollution in newborn units in Turkey. Environ Monit Assess 189, 362 (2017). https://doi.org/10.1007/s10661-017-6051-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10661-017-6051-y

Keywords

Search

Navigation