Sampling and Characterization of the Environmental Fungi in the Provincial Historic Archive of Pinar Del Río, Cuba

Sofia Borrego*; Alian Molina; Tamara Abrante

**Sofia Borrego*, Alian Molina and Tamara Abrante**

Volume1-Issue8
Dates: Received: 2020-11-17 | Accepted: 2020-12-15 | Published: 2020-12-16
Pages: 404-420

Abstract

It has been reported that there is a correlation between indoor airborne fungi and the biodeterioration of valuable documents in archives, libraries and museums, and that these fungi can also cause effects on human health if there are immunological problems or the time of exposure to these environments of low quality is long. The aims of this study were quantifying and characterizing the mycobiota of the indoor air in three repositories of the Provincial Historical Archive of Pinar del Río, Cuba and assessing its impact on the human health. The samplings were made in two different months corresponding to the years 2016 and 2017, one belonging to the rainy season and the other to the season of the little rain using a SAS biocollector and appropriate culture media to isolate fungi. The fungal concentrations and the Indoor/Outdoor (I/O) ratios obtained revealing that the repositories showed good quality environments. In both isolations Cladosporium was the predominant genus followed by Penicillium in the first sampling and Fusarium in the second isolation. The genera Aureobasidium, Sepedonium, Trichaegum and Wallemia were new findings for the Cuban archives. The pathogenic attributes studied showed that 30% of the isolates have spores so small that they can penetrate into the respiratory tract into the alveoli; 10.7% of the taxa obtained in the first isolation and 13.3% of the taxa detected in the second sampling also showed positive results to four virulence tests analyzed “In vitro” (growth at 37°C, hemolytic activity, phospholipase activity and respiratory tract level to which the spores can penetrate). These virulence factors (pathogenic attributes) evidence the risk that environmental fungi represent for the health of personnel in this archive.

FullText HTML FullText PDF DOI: 10.37871/jbres1172

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How to cite this article

Borrego S, Molina A, Abrante T. Sampling and Characterization of the Environmental Fungi in the Provincial Historic Archive of Pinar Del Río, Cuba. J Biomed Res Environ Sci. 2020 Dec 16; 1(8): 404-420. doi: 10.37871/jbres1172, Article ID: jbres1172

Subject area(s)

Microbiology

Biology

Virology

References

Borrego S, Perdomo I. Aerobiological Investigations Inside Repositories of the National Archive of the Republic of Cuba. Aerobiologia. 2012;28(3):303-316. https://bit.ly/37fYnIn
Kadaifciler DG. Bioaerosol Assessment in the Library of Istanbul University and Fungal Flora Associated with Paper Deterioration. Aerobiologia. 2017;33(1):151-166. https://bit.ly/3nhn1xW
Okpalanozie OE, Adebusoye SA, Troiano F, Cattò C, Ilori MO, Cappitelli F. Assessment of Indoor Air Environment of a Nigerian Museum Library and its Biodeteriorated Books Using Culture-Dependent and Independent Techniques. Int Biodeter Biodegr. 2018;132:139-149. https://bit.ly/3mkPCkp
Lavín P, Gómez de Saravia SG, Guiamet P. An Environmental Assessment of Biodeterioration in Document Repositories. Biofouling. 2014;30(5):561-569. https://bit.ly/3qQBB1w
Skóra J, Gutarowska B, Pielech-Przybylska K, Stępień Ł, Pietrzak K, Piotrowska M, Pietrowski P. Assessment of Microbiological Contamination in the Work Environments of Museums, Archives and Libraries. Aerobiologia. 2015;31:389-401. https://bit.ly/2K1c59g
Rahmawati SL, Zakaria L, Rahayu ES. The Diversity of Indoor Airborne Molds Growing in the University Libraries in Indonesia. Biodiversitas. 2018;19(1):194-201. https://bit.ly/2W8S6YK
Sullivan TS, Ramkissoon S, Garrison VH, Ramsubhag A, Thies JE. Siderophore Production of African Dust Microorganisms over Trinidad and Tobago. Aerobiologia. 2012;28(3):391-401. https://bit.ly/3gM8SGk
Micheluz A, Manente S, Prigione V, Tigini V, Varese GC, Ravagnan G. The Effects of Book Disinfection to the Airborne Microbiological Community in a Library Environment. Aerobiologia. 2018;34:29-44. https://bit.ly/3oQ1756
Heitman J. Microbial Pathogens in the Fungal Kingdom. Fungal Biol Rev. 2011 Mar 1;25(1):48-60. doi:10.1016/j.fbr.2011.01.003. PMID: 21528015;PMCID: PMC3081590.
Yang C, Pakpour S, Klironomos J, Li DW. Microfungi in Indoor Environments: What is Known and What is Not. In:Li DW. (Ed.), Biology of Microfungi. Switzerland: Springer International Publishing; 2016. p. 373-412. https://bit.ly/37dgvT8
Dey D, Ghosal K, Bhattacharya SG. Aerial Fungal Spectrum of Kolkata, India, Along with their Allergenic Impact on the Public Health: A Quantitative and Qualitative Evaluation. Aerobiologia. 2019;35:15-25. https://bit.ly/2LyeCbs
Suchonwanit P, Chaiyabutr C, Vachiramon V. Primary Cutaneous Chrysosporium Infection following Ear Piercing: A Case Report. Case Rep Dermatol. 2015 Jul 7;7(2):136-40. doi:10.1159/000436989. PMID: 26269703;PMCID: PMC4519602.
Andrianaki AM, Kyrmizi I, Thanopoulou K, Baldin C, Drakos E, Soliman SSM, Shetty AC, McCracken C, Akoumianaki T, Stylianou K, Ioannou P, Pontikoglou C, Papadaki HA, Tzardi M, Belle V, Etienne E, Beauvais A, Samonis G, Kontoyiannis DP, Andreakos E, Bruno VM, Ibrahim AS, Chamilos G. Iron restriction inside macrophages regulates pulmonary host defense against Rhizopus species. Nat Commun. 2018 Aug 20;9(1):3333. doi:10.1038/s41467-018-05820-2. Erratum in:Nat Commun. 2018 Nov 22;9(1):5015. PMID: 30127354;PMCID: PMC6102248.
Borrego S, Molina A. Determination of Viable Allergenic Fungi in the Documents Repository Environment of the National Archive of Cuba. Austin J Public Health Epidemiol. 2018;5(3):1077. https://bit.ly/2IKKUii
Borrego, S, Molina A, Santana A. Fungi in Archive Repositories Environments and the Deterioration of the Graphics Documents. EC Microbiol. 2017;11(5):205-226. https://bit.ly/349zcFj
Borrego S, Perdomo I. Airborne microorganisms cultivable on naturally ventilated document repositories of the National Archive of Cuba. Environ Sci Pollut Res Int. 2016 Feb;23(4):3747-57. doi:10.1007/s11356-015-5585-1. Epub 2015 Oct 24. PMID: 26498813.
Borrego S, Molina A. Behavior of the Cultivable Airborne Mycobiota in Air-Conditioned Environments of Three Havanan Archives, Cuba. Journal of Atmospheric Science Research. 2020;3(1):16-28. https://bit.ly/3a7Njil
Sánchis J. Los Nueve Parámetros Más Críticos en el Muestreo Microbiológico del Aire. Rev Tecn Lab. 2002;276:858-862. https://bit.ly/2K1XSc7
Sánchez KC, Almaguer M, Pérez I, Rojas TI, Aira MJ. Diversidad Fúngica en la Atmósfera de la Habana (Cuba) Durante Tres Períodos Poco Lluviosos. Rev Int Contam Ambie. 2019;35(1):137-150. https://bit.ly/3qSrWHR
Barnett HL, Hunter BB. Illustrated Genera of Imperfect Fungi. 4th ed. Minneapolis: Burgués; 2003. https://bit.ly/3gIggm8
Domsch KH, Gams W, Anders TH. (Eds.). Compendium of Soil Fungi. Vol. 1. London: Academic Press LTD; 1980. https://bit.ly/38gnRVx
Klich MA, Pitt JI. A Laboratory Guide to the Common Aspergillus Species and their Teleomorphs. North Ryde, New South Wales, Australia: Commonwealth Scientific and Industrial Research Organization. 1994.
Pitt JI. A Laboratory Guide to Common Penicillium Species. 3rd ed. North Ryde, New South Wales, Australia: Food Science. 2000.
Ellis MB. More Dematiaceous Hyphomycetes. Kew, Surrey, England: Commonwealth Mycological Institute. 1976. https://bit.ly/3a8KzkP
Bensch K, Groenewald JZ, Dijksterhuis J, Starink-Willemse M, Andersen B, Summerell BA, Shin HD, Dugan FM, Schroers HJ, Braun U, Crous PW. Species and ecological diversity within the Cladosporium cladosporioides complex (Davidiellaceae, Capnodiales). Stud Mycol. 2010;67:1-94. doi:10.3114/sim.2010.67.01. PMID: 20877444;PMCID: PMC2945380.
Both C. Fusarium. Laboratory Guide to the Identification of the Major Species. Kew, England: Commonwealth Mycological Institute. 1977. https://bit.ly/34b7qZ5
Smith G. Ecology and Field Biology. 2nd ed. New York: Harper & Row; 1980. https://bit.ly/3oSf6Hw
Esquivel PP, Mangiaterra M, Giusiano G, Sosa MA. Microhongos Anemófilos en Ambientes Abiertos de Dos Ciudades del Nordeste Argentino. Bol Micol. 2003;18:21-28. https://bit.ly/3qRlKjb
Bogomolova EV, Kirtsideli I. Airborne Fungi in Four Stations of the St. Petersburg Underground Railway System. Int Biodeter Biodegr. 2009;63(2):156-160. https://bit.ly/3gIbUeS
Grbić ML, Stupar M, Vukojević J, Maričić I, Bungur N. Molds in Museum Environments: Biodeterioration of Art Photographs and Wooden Sculptures. Arch Biol Sci Belgrade. 2013;65(3):955-962. https://bit.ly/2K20iYf
Fog Nielsen K. Mycotoxin production by indoor molds. Fungal Genet Biol. 2003 Jul;39(2):103-17. doi:10.1016/s1087-1845(03)00026-4. PMID: 12781669.
Zerek BF. Shortmo uldre View. In: The Preservation and Protection of Library Collections. A Practical Guide to Microbiological Controls. Chandos Publishing, Elsevier Ltd; 2014. p. 23-96. https://bit.ly/37fmlmW
Karbowska-Berent J, Gorny RL, Strzelczyk AB, Wlazło A. Airborne and Dust Borne Microorganisms in Selected Polish Libraries and Archives. Build Environ. 2011;46:1872-1879. https://bit.ly/3a4OI9r
Rodríguez JC, Rodríguez B, Borrego S. Evaluación de la Calidad Micológica Ambiental del Depósito de Fondos Documentales del Museo Nacional de la Música de Cuba en Época de Lluvia. AUMGMDOMUS. 2014;6:123-146. https://bit.ly/3nhvQb2
Stryjakowska-Sekulska M, Piotraszewska-Pająk A, Szyszka A, Nowicki M, Filipiak M. Microbiological Quality of Indoor Air in University Rooms. Pol J Environ Stud. 2007;16(4):623-632. https://bit.ly/3gLHpEJ
Salonen H, Duchaine C, Mazaheri M, Clifford S, Morawska L. Airborne Culturable Fungi in Naturally Ventilated Primary School Environments in a Subtropical Climate. Atmos Environ. 2015;106:412-418. https://bit.ly/3nhw6H2
Pyrri I, Tripyla E, Zalachori A, Chrysopoulou M, Parmakelis A, Kapsanaki-Gotsi E. Fungal Contaminants of Indoor Air in the National Library of Greece. Aerobiologia. 2020; doi: 10.1007/s10453-020-09640-0.
Cabral JP. Can we use indoor fungi as bioindicators of indoor air quality? Historical perspectives and open questions. Sci Total Environ. 2010 Sep 15;408(20):4285-95. doi:10.1016/j.scitotenv.2010.07.005. Epub 2010 Jul 23. PMID: 20655574.
Sobral LV, Melo KN, Souza CM, Silva SF, Silva GLR, Silva ALF, Wanderley KAA, Oliveira IS, Cruz R. Antimicrobial and enzymatic activity of anemophilous fungi of a public university in Brazil. An Acad Bras Cienc. 2017;89(3 Suppl):2327-2340. doi:10.1590/0001-3765201720160903. Epub 2017 Oct 26. Erratum in:An Acad Bras Cienc. 2018 Jul-Sep;90(3):3223-3239. PMID: 29091106.
Borrego S, Molina A. (2019). Fungal Assessment on Storerooms Indoor Environment in the National Museum of Fine Arts, Cuba. Air Qual Atmos Health. 2019;12:1373-1385. https://bit.ly/37YPEJK
Pinzari F. Microbial Ecology of Indoor Environments. The Ecological and Applied Aspects of Microbial Contamination in Archives, Libraries and Conservation Environments. In: Abdul-Wahab SA. (Ed.). Sick Building Syndrome in Public Buildings and Workplaces. Springer Berlin Heidelberg; 2011. pp. 153-178. https://bit.ly/3mc4Qbr
Rojas TI, Aira MJ, Batista A, Cruz IL, González S. Fungal Biodeterioration in Historic Buildings of Havana, Cuba. Grana. 2012;51(1):44-51. https://bit.ly/3qNFBjg
Roussel S, Reboux G, Millon L, Parchas MD, Boudih S, Skana F, Delaforge M, Rakotonirainy MS. Microbiological evaluation of ten French archives and link to occupational symptoms. Indoor Air. 2012 Dec;22(6):514-22. doi:10.1111/j.1600-0668.2012.00781.x. Epub 2012 Apr 18. PMID: 22429323.
Pinheiro AC, Sequeira SO, Macedo MF. Fungi in archives, libraries, and museums:a review on paper conservation and human health. Crit Rev Microbiol. 2019 Sep-Nov;45(5-6):686-700. doi:10.1080/1040841X.2019.1690420. Epub 2019 Dec 9. PMID: 31815562.
Micheluz A, Manente S, Tigini V, Prigione V, Pinzari F, Ravagnan G, Varese GC. The Extreme Environment of a Library:Xerophilic Fungi Inhabiting Indoor Niches. Int Biodeter Biodegr. 2015;99:1-7. https://bit.ly/2We9qeY
Leite-Jr DP, Pereira RS, Almeida WS, Simões SAA, Yamamoto ACA., Souza JVR, et al. Indoor air mycological survey and occupational exposure in libraries in Mato Grosso-Central Region-Brazil. Advances in Microbiology. 2018;8:324-353. https://bit.ly/37g5PmV
de Hoog GS, Guarro G, Gene J, Figueras MJ. Atlas of Clinical Fungi. 2nd edn. España: Universidad Rovira I Virgili Reus. 2000. https://bit.ly/3mgSDlY
da Cunha KC, Sutton DA, Fothergill AW, Cano J, Gené J, Madrid H, De Hoog S, Crous PW, Guarro J. Diversity of Bipolaris species in clinical samples in the United States and their antifungal susceptibility profiles. J Clin Microbiol. 2012 Dec;50(12):4061-6. doi:10.1128/JCM.01965-12. Epub 2012 Oct 10. PMID: 23052310;PMCID: PMC3502984.
Keller MD, Bergstrom GC, Shields EJ. The aerobiology of Fusarium graminearum. Aerobiologia. 2014;30:123-136. https://bit.ly/2WexCh2
EMLab. Sepedonium sp. In: Fungal Library. EMLab P & K; 2019. https://bit.ly/3gO8HdJ
Yogo N, Shapiro L, Erlandson KM. Sepedonium intra-abdominal infection:a case report and review of an emerging fungal infection. J Antimicrob Chemother. 2014 Sep;69(9):2583-5. doi:10.1093/jac/dku138. Epub 2014 Apr 30. PMID: 24788660.
Dupont EM, Field RC, Leathers CR, Northey WT. A survey of the airborne fungi in the Albuquerque, New Mexico, metropolitan area. J Allergy. 1967 Apr;39(4):238-44. doi:10.1016/0021-8707(67)90017-2. PMID: 5228670.
Mazurkiewicz-Zapałowicz K, Wróbel M, Silicki A, Wolska M. Studies on Phytopathogenic and Saprotrophic Fungi in Rush Associations of Lake Glinno (NW Poland). Acta Mycol. 2006;41(1):125-138. https://bit.ly/3gJSnKW
Nguyen HD, Jančič S, Meijer M, Tanney JB, Zalar P, Gunde-Cimerman N, Seifert KA. Application of the phylogenetic species concept to Wallemia sebi from house dust and indoor air revealed by multi-locus genealogical concordance. PLoS One. 2015 Mar 23;10(3):e0120894. doi:10.1371/journal.pone.0120894. Erratum in:PLoS One. 2015;10(5):e0129752. PMID: 25799362;PMCID: PMC4370657.
Harkawy A, Górny RL, Ogierman L, Wlazło A, Ławniczek-Wałczyk A, Niesler A. Bioaerosol assessment in naturally ventilated historical library building with restricted personnel access. Ann Agric Environ Med. 2011;18(2):323-9. PMID: 22216807.
Gutarowska B, Skora J, Zduniak K, Rembisz D. Analysis of the sensitivity of microorganisms contaminating museums and archives to silver nanoparticles. Int Biodeter Biodegr. 2012;68:7-17. https://bit.ly/3qWJTEW
Pouranik M, Mishra G. Onychomycosis: Review. EC Microbiol. 2017;5(3):81-85.
Paiva de Carvalho H, Mesquita N, Trovão J, Fernández S, Pinheiro AC, Gomes V, et al. Fungal Contamination of Paintings and Wooden Sculptures Inside the Storage Room of a Museum: A Recurrent Norms and Reference Values Adequate? J Cult Herit. 2018;34:268-276. https://bit.ly/2Ltrak9
Yang CS, Li D-W. Ecology of Fungi in the Indoor Environment. In: Yang CS, Heinshon PA. (Eds.). Sampling and Analysis of Indoor Microorganisms. John Wiley & Sons, Inc; 2007. p. 191-214. https://bit.ly/3oTkeev
Gostinčar C, Ohm RA, Kogej T, Sonjak S, Turk M, Zajc J, Zalar P, Grube M, Sun H, Han J, Sharma A, Chiniquy J, Ngan CY, Lipzen A, Barry K, Grigoriev IV, Gunde-Cimerman N. Genome sequencing of four Aureobasidium pullulans varieties: biotechnological potential, stress tolerance, and description of new species. BMC Genomics. 2014 Jul 1;15:549. doi:10.1186/1471-2164-15-549. PMID: 24984952; PMCID: PMC4227064.
Almaguer M, Aira MJ, Rodríguez-Rajo FJ, Rojas TI. Temporal Dynamics of Airborne Fungi in Havana (Cuba) During Dry and Rainy Seasons: Influence of Meteorological Parameters. Int J Biometeorol. 2014;58:1459-1470. https://bit.ly/3gIivWR
Górny RL. Filamentous microorganisms and their fragments in indoor air--a review. Ann Agric Environ Med. 2004;11(2):185-97. PMID: 15627323.
Guild S, MacDonald M. Mould Prevention and Collection Recovery: Guidelines for Heritage Collections. Technical Bulletin No. 26. Canada: Canadian Conservation Institute (CCI). 2004. https://bit.ly/380qJpl
Green BJ, Tovey ER, Sercombe JK, Blachere FM, Beezhold DH, Schmechel D. Airborne fungal fragments and allergenicity. Med Mycol. 2006 Sep;44 Suppl 1:S245-55. doi: 10.1080/13693780600776308. PMID: 17050446.
Lin WR, Chen YH, Lee MF, Hsu LY, Tien CJ, Shih FM, Hsiao SC, Wang PH. Does Spore Count Matter in Fungal Allergy?:The Role of Allergenic Fungal Species. Allergy Asthma Immunol Res. 2016 Sep;8(5):404-11. doi:10.4168/aair.2016.8.5.404. PMID: 27334778; PMCID: PMC4921694.
Twaroch TE, Curin M, Valenta R, Swoboda I. Mold allergens in respiratory allergy:from structure to therapy. Allergy Asthma Immunol Res. 2015 May;7(3):205-20. doi:10.4168/aair.2015.7.3.205. Epub 2015 Mar 11. PMID: 25840710;PMCID: PMC4397360.
Brunke S, Mogavero S, Kasper L, Hube B. Virulence factors in fungal pathogens of man. Curr Opin Microbiol. 2016 Aug;32:89-95. doi:10.1016/j.mib.2016.05.010. Epub 2016 May 31. PMID: 27257746.
Woodcock A. Moulds and asthma:time for indoor climate change? Thorax. 2007 Sep;62(9):745-6. doi:10.1136/thx.2007.079699. PMID: 17726167;PMCID: PMC2117312.
Köhler JR, Hube B, Puccia R, Casadevall A, Perfect JR. Fungi that Infect Humans. Microbiol Spectr. 2017 Jun;5(3). doi:10.1128/microbiolspec.FUNK-0014-2016. PMID: 28597822.
Nayak AP, Green BJ, Beezhold DH. Fungal hemolysins. Med Mycol. 2013 Jan;51(1):1-16. doi:10.3109/13693786.2012.698025. Epub 2012 Jul 9. PMID: 22769586;PMCID: PMC4663657.
Ghannoum MA. Potential role of phospholipases in virulence and fungal pathogenesis. Clin Microbiol Rev. 2000 Jan;13(1):122-43, table of contents. doi:10.1128/cmr.13.1.122-143.2000. PMID: 10627494;PMCID: PMC88936.
Webb BJ, Blair JE, Kusne S, Scott RL, Steidley DE, Arabia FA, Vikram HR. Concurrent pulmonary Aspergillus fumigatus and mucor infection in a cardiac transplant recipient:a case report. Transplant Proc. 2013 Mar;45(2):792-7. doi:10.1016/j.transproceed.2012.03.056. Epub 2012 Sep 15. PMID: 23267784.
Pounder JI, Simmon KE, Barton CA, Hohmann SL, Brandt ME, Petti CA. Discovering potential pathogens among fungi identified as nonsporulating molds. J Clin Microbiol. 2007 Feb;45(2):568-71. doi:10.1128/JCM.01684-06. Epub 2006 Nov 29. PMID: 17135442;PMCID: PMC1829023.
Jeyaprakasam NK, Razak MF, Ahmad NA, Santhanam J. Determining the Pathogenic Potential of Non-sporulating Molds Isolated from Cutaneous Specimens. Mycopathologia. 2016 Jun;181(5-6):397-403. doi:10.1007/s11046-016-9984-8. Epub 2016 Feb 3. PMID: 26847667.
Theeb BO, Farooq IM, Hashim AJ. Hashim S. Purification of Hemolysin from Aspergillus fumigatus and Study its Cytotoxic Effect on Normal Cell Line (REF) in Vitro. Egypt. Acad. J. Biol. Sci., G Microbiol. 2013;5:35-43. https://bit.ly/2W9fXYi
Masaphy S, Ezra R. Targeted Inspection of Environmental Mycological Load for Mitigation of Indoor Mold Toward Improved Public Health. J Microb Biochem Technol. 2016;8(5):449-458. https://bit.ly/3qVBLVd
Oliveira M, Caramalho R. Aspergillus fumigatus:A More Airborne Particle or a Powerful Biohazard?. NACC. 2014;21:20-34. https://bit.ly/345y0D5
Pérez I, Sánchez KC. Aspectos Fisiológicos del Género Cladosporium Desde la Perspectiva de sus Atributos Patogénicos, Fitopatogénicos y Biodeteriorantes. Rev Cub Cienc Biol. 2019;7(1):1-10. https://bit.ly/2JRRIeL
Valencia-Guerrero MF, Quevedo-Hidalgo B, Franco-Correa M, Díez-Ortega H, Parra-Giraldo C.M, Rodríguez-Bocanegra MX. Evaluación de Actividades Enzimáticas de Fusarium spp., Aislados de Lesiones en Humanos, Animales y Plantas. Universitas Scientiarum. 2011;16(2):147-159. https://bit.ly/3gHoMC6