Skip to main content

Advertisement

SpringerLink
Log in

Indoor air fungal pollution of a historical museum, Egypt: a case study

  • Original Paper
  • Published:
Aerobiologia Aims and scope Submit manuscript

A Correction to this article was published on 05 February 2020

This article has been updated

Abstract

Fungi can cause serious damages to historical works of art. This study aims to evaluate fungal pollution in the indoor air environment, deposited dust and surfaces of works of art in a historic house museum “Prince’s Mohamed Ali museum”, Giza, Egypt. Fungal pollution was evaluated at six museum’s buildings differed in size, design, location and content, for 2 years of campaign. The deposited dust was collected once every 3 months, while surface swabs were collected twice, after 1 year and 2 years of exposure. Airborne fungal concentrations were evaluated using volumetric (Andersen 2 stage impactor) and gravimetric (index microbial air contamination) air samplers. Airborne fungal concentrations ranged within 47–784 CFU/m3 and 175–40,250 CFU/m2/h using volumetric and gravimetric samplers, respectively. Indoor/outdoor ratio confirmed that outdoor environment was the main source of indoor fungal pollution. The rate of deposited dust was ~ 90-folds lower indoor than outdoor. Fungal concentrations associated deposited dust ranged between 102 and 104 CFU/g, representing a cause of concern. In respect to medium type, fungal diversity profile was in order of deposited dust ≥ airborne ≥ surfaces. Alternaria, Aspergillus and Cladosporium were the common fungal taxa. Secondary and tertiary fungal colonizers were detected after 2 years of exposure, indicating the presence of adequate moisture content inside the museum. No clear relationship patterns were found between microclimatic conditions and fungal culturability. The measured indoor fungal pollution and microclimatic conditions represented a problem for works of art and early indicator for fungal accumulation and biodegradation.

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

Similar content being viewed by others

Change history

  • 05 February 2020

    The article Indoor air fungal pollution of a historical museum, Egypt: a case study, written by Abdel Hameed A. Awad, Yuosra Saeed, Alia A. Shakour, Nasser M. Abdellatif, Yasser H. Ibrahim, Manal Elghanam and Fatma Elwakeel was originally published electronically on the publisher’s Internet portal <ExternalRef><RefSource>https://doi.org/10.1007/s10453-019-09623-w</RefSource><RefTarget Address="10.1007/s10453-019-09623-w" TargetType="DOI"/></ExternalRef> on 02 January 2020 with open access.

References

  • ACGIH. (1999). Bioaerosols: Assessment and control. Cincinnati, OH: American Conference of Governmental Industrial Hygienists (ACGIH).

    Google Scholar 

  • Adams, G., Gottwald, T., & Leach, C. (1986). Environmental factors initiating liberation of conidia of powdery mildews. Phytopathology,76(11), 1239–1245.

    Google Scholar 

  • AIHA, American Industrial Hygiene Association. (1989). The practitioner’s approach to IAQ investigation. In D.M. Weekes, R. B. Gammage (Eds.), Proceedings of the indoor air quality—International symposium, May 23, 1989, St. Louis, USA, Fairfax (p. 43, 66).

  • Ammar, M. S., Louboudy, S. S., & Abdul- Raouf, U. M. (1991). Distribution, total viable bacteria and identification of the most potent proteolytic bacterial strains isolated from Aswan city. Azhar Journal of Microbiology,11, 224–238.

    Google Scholar 

  • Anaf, W., Horemans, B., Madeira, T. I., Carvalho, M. L., De Wael, K., & Van Grieken, R. (2013). Effects of a constructional intervention on airborne and deposited particulate matter in the Portuguese National Tile Museum, Lisbon. Environmental Science Pollution Research,20, 1849–1857.

    CAS  Google Scholar 

  • Andersen, A. A. (1958). New sampler for the collection, sizing, and enumeration of viable airborne particles. Journal of Bacteriology,6, 471–484.

    Google Scholar 

  • Barnes, C., Tuck, J., Simon, S., Pacheco, F., Hu, F., & Portnoy, J. (2001). Allergenic materials in the house dust of allergy clinic patients. Annals of Allergy, Asthma & Immunology,86, 517–523.

    CAS  Google Scholar 

  • Barnes, C. S., Alexis, N. E., Bernstein, J. A., Cohn, J. R., Demain, J. G., Horner, E., et al. (2013). Climate change and our environment: The effect on respiratory and allergy disease. The Journal of Allergy and Clinical Immunology: In Practice,1(2), 137–141.

    Google Scholar 

  • Barnett, H. L., & Hunter, B. B. (1999). Illustrated genera of imperfect fungi (4th ed., p. 218). St. Paul, MN: The American Phytopathological Society.

    Google Scholar 

  • Camuffo, D. (1998). Microclimate for cultural heritage (p. 415). Amsterdam: Elsevier.

    Google Scholar 

  • Camuffo, D. (2013). Microclimate for cultural heritage—Conservation, restoration and maintenance of indoor and outdoor monuments (2nd ed.). Amsterdam: Elsevier.

    Google Scholar 

  • Cowan, S. T. (1974). Cowan and Steel’s manual for the identification of medical bacteria (2nd ed., pp. 193–227). England: Cambridge University Press.

    Google Scholar 

  • Dakal, T. C., & Cameotra, S. S. (2012). Microbially induced deterioration of architectural heritages: Routes and mechanisms involved. Environmental Sciences Europe,24, 36.

    Google Scholar 

  • Dalal, L., Bhowal, M., & Kolbeude, S. (2011). Incidence of deteriorating fungi in the air inside the college libraries of Wardha city. Archives of Applied Science Research,3(5), 479–485.

    CAS  Google Scholar 

  • De Nuntiis, P., & Palla, F. (2017). Bioaerosols. In F. Palla & G. Barresi (Eds.), Biotechnology and conservation of cultural heritage (pp. 31–48). Cham: Springer.

    Google Scholar 

  • Directive, 2000/54/EC of the European Parliament and of the Council of 18 September 2000 on the protection of workers from risks related to exposure to biological agents at work. O. J. E.C. L 262/21.

  • Dong, L., Qi, J., Shao, C., Zhong, X., Gao, D., Cao, W., et al. (2016). Concentration and size distribution of total airborne microbes in hazy and foggy weather. Science of the Total Environment,541, 1011–1018.

    CAS  Google Scholar 

  • Ellis, M. B. (1971). Dematiaceous hyphomycetes (p. 608). Surrey: The Western Press Ltd.

    Google Scholar 

  • Erhardt, D., & Mecklenberg, M. (1994). Relative humidity re-examined. In A. Roy & P. Smith (Eds.), Preprints of the contributions to the Ottawa Congress, preventive conservation: Practice theory and research (pp. 32–38). London: International Institute for Conservation of Historic and Artistic Works.

    Google Scholar 

  • Flannigan, B., & Morey, P. R. (1996). Control of moisture problems affecting biological indoor air quality. ISIAQ, International Society of Indoor Air Quality and Climate Guideline TFI-1996, Ottawa, Canada.

  • Godish, D., & Godish, T. (2007). Relationship between sampling duration and concentration of culturable airborne mould and bacteria on selected culture media. Journal of Applied Environmental Microbiology,102, 1479–1484.

    CAS  Google Scholar 

  • Górny, A. R., Harkawy, A., Lawniczek-Walczyk, A., Karbowska-Berent, J., Wlazlo, A., Nielsler, A., et al. (2016). Exposure to culturable and total microbiota in cultural heritage conservation laboratories. International Journal of Occupational Medicine and Environmental Health,29(2), 255–275.

    Google Scholar 

  • Grau-Bové, J., & Strlič, M. (2013). Fine particulate matter in indoor cultural heritage: A literature review. Heritage Science,1, 1–17.

    Google Scholar 

  • Gutarowska, B. (2010). Metabolic activity of moulds as a factor of building biodegradation. Polish Journal of Microbiology,59(2), 119–124.

    CAS  Google Scholar 

  • Humphreys, H. (1992). Microbes in the air—When to count (the role of air sampling in hospitals). Journal of Medical Microbiology,37, 81–82.

    CAS  Google Scholar 

  • ISO 14698-1. (2003). Clean rooms and associated controlled environments—Biocontamination control. Part 1: General principles and methods. https://www.iso.org/standard/25015.html. Accessed 3 Jan 2019.

  • Karbowska-Berent, J., Górny, R. L., Strelczyk, A. B., & Wlazío, A. (2011). Airborne and dustborne microorganisms in selected Polish libraries and archives. Building and Environment,46, 1872–1879.

    Google Scholar 

  • Krakoval, L., Chovanova, K., Selim, S. A., Simonovicova, A., Puskarova, A., Makova, A., et al. (2012). A multiphasic approach for investigation of microbial diversity and its biodegradative abilities in historical paper and parchment documents. International Biodeterioration and Biodegradation,70, 117–125.

    Google Scholar 

  • Lacey, J. (1991). Aggregation of spores and its effect on aerodynamic behavior. Grana,30, 437–445.

    Google Scholar 

  • Lazaridis, M., Katsivela, E., Kopanakis, I., Raisi, L., & Panagiaris, G. (2015). Indoor/outdoor particulates matter concentrations and microbial load in cultural heritage collections. Heritage Science,3(1), 3–34.

    Google Scholar 

  • Lech, T. (2015). Molecular biology methods to assess microbiological hazard concerning objects of cultural heritage. British Microbiology Research Journal,9(6), 1–9.

    CAS  Google Scholar 

  • Lopez-Miras, M., Pinar, G., Romero-Noguera, J., Bolıvar-Galiano, F. C., Ettenauer, J., Sterflinger, K., et al. (2013). Microbial communities adhering to the obverse and reverse sides of an oil painting on canvas: Identification and evaluation of their biodegradative potential. Aerobiologia,29, 301–314.

    CAS  Google Scholar 

  • Mammarella, L. (1971). Inquinamenti Dell’aria. Roma: II Pensiero Scientifico.

    Google Scholar 

  • May, E., Lewis, F. J., Pereira, S., Tayler, S., Seaward, M. R. D., & Allsopp, D. (1993). Microbial deterioration of building stone—A review. Biodeterioration Abstracts,7, 109–123.

    Google Scholar 

  • MIBAC—The Italian Ministry of Cultural Heritage. (1998). Official guidelines on technical-scientific criteria and standards of operation and development of museums. Scope VI. J Laws No. 150(6). Italian.

  • Montenecourt, B. S., & Eveleigh, D. E. (1977). Semi quantitative plate assay for determination of cellulase production by Trichoderma viride. Journal Applied Environmental Microbiology,33(1), 178–183.

    CAS  Google Scholar 

  • Osman, M. E., Om Kalthoum, H. K., & El-Shaphy, A. A. (2008). Production of cellulase and pectinase from some aquatic hyphomycetes. Research Journal of Microbiology,3, 213–224.

    CAS  Google Scholar 

  • Parchas, M.-D. (2008). How to deal with biohazards?. Paris: Direction des Archives de France.

    Google Scholar 

  • Pasanen, A., Kasanen, J., Rautiala, S., Ikaheimo, M., Rantamaki, J., Kaariainen, H., et al. (2000). Fungal growth and survival in building materials under fluctuating moisture and temperature conditions. International Biodeterioration and Biodegradation,46, 117–127.

    Google Scholar 

  • Pasquarella, C., Pitzurrat, O., & Savino, A. (2000). The index of microbial air contamination. Journal of Hospital Infection,46, 241–256.

    CAS  Google Scholar 

  • Pelczar, M. J., Chan, E. C. S., & Krieg, N. R. (1996). Microbioolgy: Concepts and applications (p. 796). New York: McGraw Hill Inc.

    Google Scholar 

  • Pitt, I. J., & Hocking, A. (2009). Fungi and food spoilage. New York: Springer.

    Google Scholar 

  • Portnoy, J. M., Barnes, C. S., & Kennedy, K. (2004). Sampling for indoor fungi. Journal of Allergy and Clinical Immunology,113, 189–198.

    Google Scholar 

  • Raper, K. B., & Fennell, D. I. (1977). The genus Aspergillus. Huntington: R. E. Krieger Publishing Company.

    Google Scholar 

  • Reponen, T., Willeke, K., Grinshpun, S., & Nevalanen, A. (2001). Biological particles sampling. In P. Baron & K. Willeke (Eds.), Aerosol measurement: Principles, techniques and applications (2nd ed.). New York: Wiley.

    Google Scholar 

  • Ritschkoff, A. C., Viitanen, H., & Koskela, K. (2000). The response of building materials to the mould exposure at different humidity and temperature conditions. In: O. Seppänen, & J. Säteri (Eds.), Healthy Buildings 2000, Vol. 1, 6–10 August, Finnish Society of Indoor Air Quality and Climate (FiSIAQ), Espoo, FI (pp. 317–322).

  • Rylander, R., & Jacobs, R. R. (1994). Organic dusts, exposure, effects and prevention. Boca Raton, FL: CRC Press Inc.

    Google Scholar 

  • Sablier, M., & Garrigues, P. (2014). Cultural heritage and its environment: an issue of interest for Environmental Science and Pollution Research. Environmental Science and Pollution Research,21(9), 5769–5773.

    Google Scholar 

  • Sarica, S. Ö., Asan, A., Tungan, Y., & Ture, M. (2005). Airborne fungal concentrations in east patch of Edirne City (Turkey) in autumn using two sampling methods. Trakya University Journal of Science,6(1), 97–106.

    Google Scholar 

  • Sharpe, R. A., Bearman, N., Thornton, C. R., Husk, K., & Osborne, N. J. (2015). Indoor fungal diversity and asthma: A meta-analysis and systematic review of risk factors. Journal of Allergy and Clinical Immunology,135(1), 110–122.

    Google Scholar 

  • Shelton, B. G., Kirkland, K. H., Flanders, W. D., & Morris, G. K. (2002). Profiles of airborne fungi in buildings and outdoor environments in the United States. Applied and Environmental Microbiology,68(4), 1743–1753.

    CAS  Google Scholar 

  • Sindt, C., Besancenot, J. P., & Thibaudon, M. (2016). Airborne Cladosporium fungal spores and climate change in France. Aerobiologia,32(1), 53–68.

    Google Scholar 

  • Singh, K., Frisvad, J. C., Thrane, U., & Mathur, S. B. (1991). An illustrated manual on identification of some seed-borne Aspergilli, Fusaria, Penicillia and their mycotoxins. Denmark, Danish Government Institute of Seed Pathology for Developing Countries.

  • Singh, R. N., Gupta, V. K., & Goswami, G. R. (2006). A simple activity staining protocol for lipases and esterases. Applied Microbiology and Biotechnology,70, 679–682.

    CAS  Google Scholar 

  • Skóra, J., Gutarowska, B., Pielech-Przybylska, K., Stępień, Ł., Pietrzak, K., Piotrowska, M., et al. (2015). Assessment of microbiological contamination in the work environments of museums, archives and libraries. Aerobiologia,31(3), 389–401.

    Google Scholar 

  • Sterflinger, K. (2010). Fungi: their role in deterioration of cultural heritage. Fungal Biology Reviews,24, 47–55.

    Google Scholar 

  • Sterflinger, K., & Piñar, G. (2013). Microbial deterioration of cultural heritage and works of art—Tilting at windmills? Applied Microbiology and Biotechnology,97(22), 9637–9646.

    CAS  Google Scholar 

  • Urzi, C., De Leo, F., Salamone, P., & Criseo, G. (2001). Airborne fungal spores colonizing marbles exposed in the terrace of Messina Museum, Sicily. Aerobiologia,17, 11–17.

    Google Scholar 

  • Urzi, C., & Realini, M. (1998). Colour changes of Noto, s calcareous sandstone as related to its colonization by microorganisms. International Biodeterioration and Biodegradation,42, 45–54.

    Google Scholar 

  • WHO, World Health Organization. (2009). WHO guidelines for indoor air quality: Dampness and mould. Bonn: WHO. 2009. Retrieved December 2, 2018 from http://www.euro.who.int/__data/assets/pdf_file/0017/43325/E92645.pdf.

  • Whyte, W. (1995). Sterility assurance and models for assessing bacterial contamination. Journal of Parenteral Science and Technology,40, 188–197.

    Google Scholar 

  • Yilmazkaya, D., Tosunoghu, A., Akgul, H., & Bicakci, A. (2018). Dominated airborne fungal spores in Hatay, Turkey: The eastern coast of the Mediterranean basin. In The proceeding of ICB2018, 11th international congress on aerobiology, September 3–7, 2018, Parma, Italy (p. 151).

  • Yu, J., Hu, Q., Xie, Z., Kang, H., Li, M., Li, Z., et al. (2013). Concentration and size distribution of fungi aerosol over oceans along a cruise path during the fourth Chinese arctic research expedition. Atmosphere,4(4), 337–348.

    Google Scholar 

  • Zhai, Y., Li, X., Wang, T., Wang, B., Li, C., & Zeng, G. (2018). A review on airborne microorganisms in particulate matters: composition, characteristics and influence factors. Environment International,113, 74.

    Google Scholar 

  • Żukiewicz-Sobczak, W. A. (2013). The role of fungi in allergic diseases. Postepy Dermatologii I Alergologii,30(1), 42–45.

    Google Scholar 

Download references

Acknowledgements

This study was funded by Research Grant No. 11070108 from the National Research Centre, Dokki, Giza, Egypt.

Author information

Authors and Affiliations

  1. Air Pollution Research Department, National Research Centre, P.O. 12622, Dokki, Giza, Egypt

    Abdel Hameed A. Awad, Yuosra Saeed, Alia A. Shakour, Nasser M. Abdellatif & Yasser H. Ibrahim

  2. Restoration and Conservation Department, National Museum of Egyptian Civilization, Cairo, Egypt

    Manal Elghanam & Fatma Elwakeel

Authors
  1. Abdel Hameed A. Awad
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yuosra Saeed
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alia A. Shakour
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nasser M. Abdellatif
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yasser H. Ibrahim
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Manal Elghanam
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Fatma Elwakeel
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Abdel Hameed A. Awad.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

The original version of this article was revised due to retrospective Open Access cancellation.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Awad, A.H.A., Saeed, Y., Shakour, A.A. et al. Indoor air fungal pollution of a historical museum, Egypt: a case study. Aerobiologia 36, 197–209 (2020). https://doi.org/10.1007/s10453-019-09623-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10453-019-09623-w

Keywords

Search

Navigation