Behavior of the Cultivable Airborne Mycobiota in Air-Conditioned Environments of Three Havanan Archives, Cuba

Sofia Flavia Borrego Alonso (Preventive Conservation Laboratory, National Archive of the Republic of Cuba, Compostela 906 esquina a calle San Isidro, PO Box: 10100, La Habana Vieja, Havana, Cuba.)
Alian Molina (Preventive Conservation Laboratory, National Archive of the Republic of Cuba, Compostela 906 esquina a calle San Isidro, PO Box: 10100, La Habana Vieja, Havana, Cuba.)


High concentrations of environmental fungi in the archives repositories are dangerous for the documents preserved in those places and for the workers' health. The aims of this work were to evaluate the behavior of the fungal concentration and diversity in the indoor air of repositories of 3 archives located in Havana, Cuba, and to demonstrate the potential risk that these taxa represent for the documentary heritage preserved in these institutions. The indoor and outdoor environments were sampled with a biocollector. From the I/O ratios, it was evident that two of the studied archives were not contaminated, while one of them did show contamination despite having temperature and relative humidity values very similar to the other two. Aspergillus, Penicillium and Cladosporium were the predominant genera in the indoor environments. New finds for archival environments were the genera Harposporium and Scolecobasidium. The principal species classified ecologically as abundant were C. cladosporioides and P. citrinum. They are known as opportunistic pathogenic fungi. All the analyzed taxa excreted acids, the most of them degraded cellulose, starch and gelatin while about 48% excreted different pigments. But 33% of them showed the highest biodeteriogenic potential, evidencing that they are the most dangerous for the documentary collections.


Archives;Environmental fungi;Indoor environments;Microbial quality of archive environments;Quality of indoor environments;Documentary biodeterioration

Full Text:



[1] Pinzari F. Microbial ecology of indoor environments. The ecological and applied aspects of microbial contamination in archives, libraries and conservation environments. In Sick Building Syndrome in public buildings and workplaces, pp 153-178, Abdul-Wahab AA (ed.). Springer Berlin Heidelberg, 2011, DOI: 10.1007/978-3-642-17919-8_9.

[2] Lavín P, Gómez de Saravia SG, Guiamet P. An environmental assessment of biodeterioration in document repositories. Biofouling, 2014, 30(5): 561-569, DOI: 10.1080/08927014.2014.897334.

[3] Kadaifciler GD. Bioaerosol assessment in the library of Istanbul University and fungal flora associated with paper deterioration. Aerobiologia, 2017, 33(1): 151-166, DOI: 10.1007/s10453-016-9457-z.

[4] Górny RL. Filamentous microorganisms and their fragments in indoor air. Ann Agric Environ Med., 2004, 11:185-197.

[5] Anaya M, Borrego SF, Gámez E, Castro M, Molina A, Valdés O. Viable fungi in the air of indoor environments of the National Archive of the Republic of Cuba. Aerobiologia, 2016, 32(3):513-527, DOI: 10.1007/s10453-016-9429-3.

[6] Górny RL, Harkawy AS, Ławniczek-Wałczyk A, Karbowska-Berent J, Wlazło A, Niesler A, et al. Exposure to culturable and total microbiota in cultural heritage conservation laboratories. Int J Occup Med Environ Health., 2016, 29(2): 255-275, DOI: 10.13075/ijomeh.1896.00630.

[7] 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 Biodeterior Biodegr., 2018, 132: 139-149, DOI: 10.1016/j.ibiod.2018.03.003.

[8] Elenjikamalil SMR, Kelkar-Mane V. Seasonal variations in the aerobiological parameters of a state archival repository in India. World J Pharm Res., 2019, 8(5): 1459-1474, DOI: 10.20959/wjpr20195-14734.

[9] Guiamet PS, Borrego S, Lavin P, Perdomo I, Gómez de Saravia S. Biofouling and biodeterioration in material stored at the Historical Archive of the Museum of La Plata, Argentine and at the National Archive of the Republic of Cuba. Colloid Surface B., 2011, 85(2): 229-234, DOI: 10.1016/j.colsurfb.2011.02.031.

[10] Rodríguez JC. Evaluación aeromicrobiológica del depósito del Centro de Documentación del Museo Nacional de la Música de Cuba. Ge-conservación, 2016, (9): 117-126.

[11] Unković N, Dimkić I, Stanković S, Jelikić A, Stanojević D, Popović S, et al. Seasonal diversity of biodeteriogenic, pathogenic, and toxigenic constituents of airborne mycobiota in a sacral environment. Arh Hig Rada Toksikol., 2018, 69: 317-327, DOI: 10.2478/aiht-2018-69-3194.

[12] Borrego S, Molina A. Fungal assessment on storerooms indoor environment in the National Museum of Fine Arts, Cuba. Air Qual Atmos Health., 2019, 12: 1373-1385, DOI: 10.1007/s11869-019-00765-x.

[13] Cabral JPS. Can we use indoor fungi as bioindicators of indoor air quality? Historical perspectives and open questions. Sci Total Environ., 2010, 408(20): 4285-4295, DOI: 10.1016/j.scitotenv.2010.07.005.

[14] Haleem-Khan AA, Mohan-Karuppayil S. Fungal pollution of indoor environments and its management. Saudi J Biol Sci., 2012, 19: 405-426, DOI: 10.1016/j.sjbs.2012.06.002.

[15] Roussel S, Reboux G, Millon L, Parchas MD, Boudih S, Skana F, et al. Microbiological evaluation of ten French archives and link to occupational symptoms. Indoor Air, 2012, 22(6): 514-522, DOI: 10.1111/j.1600-0668.2012.00781.x.

[16] Köhler JR, Hube B, Puccia R, Casadevall A, Perfect JR. Fungi that infect humans. In The Fungal Kingdom, pp 813-843. Heitman J, Howlett BJ, Crous PW, Stukenbrock EH, James TY, Gow NAR (eds). Washington: American Society for Microbiology, 2018, DOI: 10.1128/microbiolspec.FUNK-0014-2016.

[17] Sanchis J. Los nueve parámetros más críticos en el muestreo biológico del aire. Rev Tecn Lab., 2002, 276: 858-862.

[18] Almaguer M, Rojas-Flores TI. Aeromicota viable de la atmósfera de La Habana, Cuba. Nova Acta Científica Compostelana (Bioloxía), 2013, 20: 35-45.

[19] Borrego S, Perdomo I. Airborne microorganisms cultivable on naturally ventilated document repositories of the National Archive of Cuba. Environ Sci Pollut Res., 2016, 23(4): 3747-3757, DOI: 10.1007/s11356-015-5585-1.

[20] Borrego S, Molina A, Santana A. Fungi in archive repositories environments and the deterioration of the graphics documents. EC Microbiology, 2017, 11(5): 205-226.

[21] Aschner M, Kohn S. The Biology of Harposporium anguillulae. J Gen Mirobiol., 1958, 19: 182-189.

[22] De Hoog GS. The genera Beauveria, Isaria, Tritirachium and Acrodontium gen. nov. Stud Mycol., 1972, 1: 1-41.

[23] Ellis MB. More Dematiaceous hyphomycetes. England: Commonwealth Mycological Institute, 1976.

[24] Brayford D. CMI Descriptions of pathogenic fungi and bacteria no. 926. Cylindrocarpon lichenicola. Mycopathologia, 1987, 100(2): 125-126.

[25] Barnett HL, Hunter BB. Illustrated genera of Imperfect fungi. 4th edn. Minneapolis: APS Press, 1998.

[26] Klich MA, Pitt JI. A laboratory guide to the common Aspergillus species and their teleomorphs, Australia: CSIRO, Division of Food Processing, 1994.


[28] Piontelli E. Agentes comunes en las aspergilosis humanas: conceptos primarios en la diferenciación de sus complejos de especies. Bol Micol., 2014, 29(2): 63-100.

[29] Pitt JI. A laboratory guide to common Penicillium species. 3rd ed. Australia: CSIRO, Division of Food Processing, 2000.

[30] Wang CY, Mo MH, Li X, Tian BY, Zhang KQ. Morphological characteristics and infection processes of nematophagous Harposporium with reference to two new species. Fungal Diversity, 2007, 26: 287-304.

[31] Bensch K, Braun U, Groenewald JZ, Crous PW. The genus Cladosporium. Stud Mycol., 2012, 72: 1-401, DOI: 10.3114/sim.2010.67.01.

[32] Smith G. Ecology and Field Biology, 2nd edn. New York: Harper & Row, 1980.

[33] 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.

[34] Bogomolova EV, Kirtsideli I. Airborne fungi in four stations of the St. Petersburg underground railway system. Int Biodeter Biodegr., 2009, 63(2): 156-160, DOI: 10.1016/j.ibiod.2008.05.008.

[35] Ponnambalam A, Deepthi R, Ghosh A. Qualitative display and measurement of enzyme activity of isolated cellulolytic bacteria. Biotechnol Bioinf Bioeng., 2011, 1(1): 33-37.

[36] Ahmad B, Nigar S, Shah SA, Bashir S, Ali J, Yousaf S, Bangash JA. Isolation and identification of cellulose degrading bacteria from municipal waste and their screening for potential antimicrobial activity. World Appl Sci J., 2013, 27(11): 1420-1426, DOI: 10.5829/idosi.wasj.2013.27.11.81162.

[37] Borrego S, Guiamet P, Gómez de Saravia S, Batistini P, Garcia M, Lavin P, Perdomo I. The quality of air at archives and the biodeterioration of photographs. Int Biodeter Biodegr., 2010, 64(2): 139-145, DOI: 10.1016/j.ibiod.2009.12.005.

[38] Iwatzu T. A new species of Cladosporium from Japan. Mycotaxon, 1984, 20: 521-533.

[39] Molina A, Borrego SF, Análisis de la micobiota existente en el ambiente interior de la Mapoteca del Archivo Nacional de la República de Cuba. Bol Micol., 2014, 29(1): 2-17.

[40] Luo Y, Li J, Zhang X, Gao W. Characterization of potential pathogenic Cladosporium exposure risks from heating, ventilation and air conditioning (HVAC) in two cities, China. Med Mycol Open Access, 2016, 2(18): 1-8, DOI: 10.21767/2471-8521.100018.

[41] 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, DOI: 10.4236/aim.2018.84022.

[42] Chaudhuri A, Bhattacharyya S. Foldscopic visualization and identification of airborne fungi in museum and library environment. Journal of Emerging Technologies and Innovative Research, 2019, 6(6): 838-841.

[43] 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): 323-329.


[45] Báez-Flores ME, Medina PG, Díaz-Camacho SPD, de Jesús Uribe-Beltrán M, de la Cruz- Otero MC, et al. Fungal spore concentrations in indoor and outdoor air in university libraries, and their variations in response to changes in meteorological variables. Int J Environ Health Res., 2014, 24(4): 320-340, DOI: 10.1080/09603123.2013.835029.

[46] 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.

[47] Sobral LV, Melo KN, Souza CM, Silva SF, Silva GLR, Silva ALF, et al. Antimicrobial and enzymatic activity of anemophilous fungi of a public university in Brazil. An Acad Bras Cienc., 2017, 89(3 Suppl.): 2327-2356, DOI: 10.1590/0001-3765201720160903.

[48] Borrego S, Perdomo I. Aerobiological investigations inside repositories of the National Archive of the Republic of Cuba. Aerobiologia, 2012, 28(3): 303-316, DOI: 10.1007/s10453-011-9235-x.

[49] Borrego S, Lavin P, Perdomo I, Gómez de Saravia S, Guiamet P. Determination of indoor air quality in archives and biodeterioration of the documentary heritage. ISRN Microbiol., 2012, DOI: 10.5402/2012/680598.

[50] 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, DOI: 10.1016/j.atmosenv.2014.07.052.

[51] 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, DOI: 10.13057/biodiv/d190126.

[52] Pinheiro AC, Sequeira SO, Macedo MF. Fungi in archives, libraries, and museums: a review on paper conservation and human health. Crit Rev Microbiol., 2019, DOI: 10.1080/1040841X.2019.1690420.

[53] 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.

[54] Alhussaini MS, Moslem MA, Mohammed S, Alghonaim MI, Al-Ghanayem AA, Hefny HM. Biodiversity and distribution of airborne Cladosporium species in Riyadh city. J Am Sci., 2015, 11(7): 145-154.

[55] Karbowska-Berent J, Górny RL, Strzelczyk AB, Wlazło A. Airborne and dust borne microorganisms in selected Polish libraries and archives. Build Environ., 2011, 46: 1872-1879, DOI: 10.1016/j.buildenv.2011.03.007.

[56] Micheluz A, Manente S, Tigini V, Prigione V, Pinzari F, Ravagnan G, Varese G. The extreme environment of a library: Xerophilic fungi inhabiting indoor niches. Int Biodeterior Biodegr., 2015, 99: 1-7, DOI: 10.1016/j.ibiod.2014.12.012.

[57] Stevenson A, Hamill PG, O’Kane CJ, Kminek G, Rummel JD, Voytek MA, et al. Aspergillus penicillioides differentiation and cell division at 0.585 water activity. Environ Microbiol., 2017, 19(2): 687-697, DOI: 10.1111/1462-2920.13597.

[58] Borrego S, Guiamet P, Vivar I, Battistoni P. Fungi involved in biodeterioration of documents in paper and effect on substrate. Acta Microscopica, 2018, 27(1): 37- 44.

[59] Sánchez KC, Almaguer M. Aeromicología y salud humana. Revista Cubana de Medicina Tropical, 2014, 66(3): 322-337.

[60] De Hoog GS, Guarro G, Gene J, Figueras MJ. Atlas of clinical fungi, 2nd edn. Spain: Centraalbureau voor Schimmelcultures, Utrecht/Universitat Rovira i Virgili, Reus, 2000.

[61] Denning DW. Aspergilosis. UK: Schering-plough Corporation, 2006.

[62] Klich MA. Identification of clinically relevant aspergilla. Med Mycol., 2006, 44:S127-S131, DOI: 10.1080/13693780600796546.

[63] Hedayati MT, Pasqualotto AC, Warn PA, Bowyer P, Denning DW. Aspergillus flavus: Human pathogen, allergen and mycotoxin producer. Microbiology, 2007, 153(Pt 6): 1677-1692, DOI: 10.1099/mic.0.2007/007641-0.

[64] Gautan AK, Sharma S, Avasthi S, Bhadauria R. Diversity, pathogenicity and toxicology of A. niger: An important spoilage fungi. Res J Microbiol., 2011, 6(3): 270-280, DOI: 10.3923/jm.2011.270.280.

[65] Molina A, Borrego S. Aerobiología y biodeterioro del género Aspergillus Link en depósitos de tres instituciones patrimoniales cubanas. Bol Micol., 2016, 31(1): 2-18.

[66] 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, 45(2): 568-571, DOI: 10.1128/JCM.01684-06.

[67] Rodríguez-Orozco A, Vargas-Villegas E, Tafolla-Muñoz L, Ruiz-Reyes H, Hernández-Chávez LA, Vázquez-Garcidueñas S. Géneros fúngicos aislados de pacientes con rinitis alérgica y su relación con la prueba de hipersensibilidad subcutánea de prick. Rev Mex Micol., 2008, 28: 89-94.

[68] Vivar I, Borrego S, Ellis G, Moreno DA, García MA. Fungal biodeterioration of color cinematographic films of the cultural heritage of Cuba. Int Biodeter Biodegr., 2013, 84: 372-380, DOI: 10.1016/j.ibiod.2012.05.021.

[69] Borrego S, Molina A, Santana A. Mold on stored photographs and maps: A case study. Topics in Photographic Preservation, 2015, 16: 109-120.

[70] Vivar I, Borrego SF, García AM, Moreno DA. Microscopic techniques in the determination of the biodeterioration in cinematographic films. Acta Microscopica, 2018, 27(1): 63-68.

[71] Szczepanowska H, Mathia TG, Belin P. Morphology of fungal stains on paper characterized with multi-scale and multi-sensory surface metrology. Scanning, 2014, 36(1): 76-85, DOI: 10.1002/sca.21095.

[72] Szczepanowska H, Jha D, Mathia TG. Morphology and characterization of Dematiaceous fungi on a cellulose paper substrate using synchrotron X-ray microtomography, scanning electron microscopy and confocal laser scanning microscopy in the context of cultural heritage. J Anal At Spectrom., 2015, 30(3): 651-657, DOI: 10.1039/c4ja00337c.

[73] Piñar G, Tafer H, Sterflinger K, Pinzari F. Amid the possible causes of a very famous foxing: Molecular and microscopic insight into Leonardo da Vinci’s self-portrait. Environ Microbiol Rep., 2015, 7(6): 849-859, DOI: 10.1111/1758-2229.12313.

[74] Sequeira SO, Carvalho H. D, Mesquita N, Portugal A, Macedo MF. Fungal stains on paper: is what you see what you get? Conserv património, 2019, 32: 18-27, DOI: 10.14568/cp2018007.



  • There are currently no refbacks.
Copyright © 2020 Sofia Flavia Borrego Alonso

Creative Commons License
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.