Pollution of Airborne Fungi in Naturally Ventilated Repositories of the Provincial Historical Archive of Santiago de Cuba (Cuba)

Sofia Borrego (Conservation Preventive laboratory, National Archive of the Republic of Cuba, Havana city, Cuba)
Alian Molina (Conservation Preventive laboratory, National Archive of the Republic of Cuba, Havana city, Cuba)
Yuneisis Bonne (Conservation Department, Provincial Historic Archive of Santiago de Cuba, Santiago de Cuba city, Cuba)
Anyilena González (Conservation Department, Provincial Historic Archive of Santiago de Cuba, Santiago de Cuba city, Cuba)
Lidiersy Méndez (Conservation Department, Provincial Historic Archive of Santiago de Cuba, Santiago de Cuba city, Cuba)

Article ID: 4536


Environmental fungi can damage the documentary heritage conserved in archives and affect the personnel’s health if their concentrations, thermohygrometric parameters and ventilation conditions are not adequate, problems that can be accentuated by Climate Change. The aims of this work were to identify and to characterize the airborne fungal pollution of naturally ventilated repositories in the Provincial Historical Archive of Santiago de Cuba and predict the risk that these fungi pose to the staff’s health. Indoor air of three repositories of this archive and the outdoor air were sampled in an occasion every time in 2015, 2016 and 2017 using a SAS sampler. The obtained fungal concentrations varied from 135.6 CFU/m3 to 421.1 CFU/m3 and the indoor/outdoor ratios fluctuated from 0.7 to 4.2, evidencing a variable environmental quality over time, but in the third sampling the repositories environments showed good quality. Aspergillus and Cladosporium were the predominant genera in these environments. A. flavus was a prevailed species in indoor air, while A. niger and Cl. cladosporioides were the species that showed the greatest similarities with the outdoor air. Coremiella and Talaromyces genera as well as the species Aspergillus uvarum, Alternaria ricini and Cladosporium staurophorum were the first findings for environments of Cuban archives. Xerophilic species (A. flavus, A. niger, A. ochraceus, A. ustus) indicators of moisture problems in the repositories were detected; they are also opportunistic pathogens and toxigenic species but their concentrations were higher than the recommended, demonstrating the potential risk to which the archive personnel is exposed in a circumstantial way.


Archive environments; Fungal pollution; Indoor air; Environmental quality; Ventilated repositories; Toxigenic species

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[1] Pinzari, F., 2011. 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; Abdul-Wahab, SA., Ed.; Springer-Verlag Heidelberg: Berlin, Germany. pp. 153-178. DOI: https://doi.org/10.1007/978-3-642-17919-8_9

[2] Michaelsen, A., Pinzari, F., Ripka, K., et al., 2006. Application of molecular techniques for identification of fungal communities colonising paper material. International Biodeterioration and Biodegradation. 58, 133-141. DOI: https://doi.org/10.1016/j.ibiod.2006.06.019

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

[4] Pinheiro, A.C., Sequeira, S.O., Macedo, M.F., 2019. Fungi in archives, libraries, and museums: A review on paper conservation and human health. Critical Reviews in Microbiology. 45(5-6), 686-700. DOI: https://doi.org/10.1080/1040841X.2019.1690420

[5] Sequeira, S.O., Paiva de Carvalho, H., Mesquita, N., et al., 2019. Fungal stains on paper: is what you see what you get? Conservar Património. 32, 8-27. DOI: https://doi.org/10.14568/cp2018007

[6] Haleem-Khan, A.A., Mohan-Karuppayil, S., 2012. Fungal pollution of indoor environments and its management. Saudi Journal of Biological Sciences. 19, 405-426. DOI: http://dx.doi.org/10.1016/j.sjbs.2012.06.002

[7] Twaroch, T.E., Curin, M., Valenta, R., et al., 2015. Mold allergens in respiratory allergy: From structure to therapy. Allergy, Asthma and Immunology Research. 7(3), 205-220. DOI: http://dx.doi.org/10.4168/aair.2015.7.3.205

[8] Nayak, A.P., Green, B.J., Beezhold, D.H., 2013. Fungal hemolysins. Medical Mycology. 51, 1-16. DOI: https://doi.org/10.3109/13693786.2012.698025

[9] Aboul-Nasr, M.B., Zohri, A.N.A., Amer, E.M., 2013. Enzymatic and toxigenic ability of opportunistic fungi contaminating intensive care units and operation rooms at Assiut University Hospitals, Egypt. Springer Plus. 2, 347. DOI: https://doi.org/10.1186/2193-1801-2-347

[10] Oetari, A., Susetyo-Salim, T., Sjamsuridzal, W., et al. 2016. Occurrence of fungi on deteriorated old dluwang manuscripts from Indonesia. International Biodeterioration and Biodegradation. 114, 94-103. DOI: http://dx.doi.org/10.1016/j.ibiod.2016.05.025

[11] Borrego S, Molina A, Santana A. 2017. Fungi in archive repositories environments and the deterioration of the graphics documents. EC Microbiology, 11(5), 205-226. https://www.researchgate.net/publication/319713307_Fungi_in_Archive_Repositories_Environments_and_the_Deterioration_of_the_ Graphics_Documents.

[12] Borrego, S., Molina, A., 2020. Behavior of the cultivable airborne mycobiota in air-conditioned environments of three Havanan archives, Cuba. Journal of Atmospheric Science Research. 3(1), 16-28. DOI: https://doi.org/10.30564/jasr.v3i1.1910

[13] Mallo AC, Nitiu DS, Elíades LA, Saparrat MCN. 2017. Fungal degradation of cellulosic materials used as support for cultural heritage. International Journal of Conservation Science, 8(4), 619-632. http://www. ijcs.uaic.ro/public/IJCS-17-59_Mallo.pdf.

[14] Fröhlich-Nowoisky, J., Kampf, C.J., Weber, B., et al., 2016. Bioaerosols in the Earth system: Climate, health, and ecosystem interactions. Atmospheric Research. 182, 346-376. DOI: https://doi.org/10.1016/j.atmosres.2016.07.018

[15] De Nuntiis, P., Palla, F., 2017. Bioaerosols. In Biotechnology and conservation of cultural heritage; Palla, F., Barresi, G., Eds.; Springer International Publishing: Switzerland. pp. 31-48. DOI: https://doi.org/10.1007/978-3-319-46168-7_2

[16] Vardoulakis, S., Dimitroulopoulou, C., Thornes, J., et al., 2015. Impact of climate change on the domestic indoor environment and associated health risks in the UK. Environment International. 85, 299-313. DOI: https://doi.org/10.1016/j.envint.2015.09.010

[17] Panackal, A.A., 2011. Global climate change and infectious diseases: Invasive mycoses. Journal of Earth Science & Climatic Change. 1, 108. DOI: https://doi.org/10.4172/2157-7617.1000108

[18] Anaf, W., Leyva, D., Schalm, O., 2018. Standardized indoor air quality assessments as a tool to prepare heritage guardians for changing preservation conditions due to Climate Change. Geosciences. 8, 276. DOI: https://doi.org/10.3390/geosciences8080276

[19] Borrego, S., Perdomo, I., 2016. Airborne microorganisms cultivable on naturally ventilated document repositories of the National Archive of Cuba. Environmental Science and Pollution Research. 23(4), 3747-3757. DOI: https://doi.org/10.1007/s11356-015-5585-1

[20] Borrego S, Molina A. 2018. Determination of viable allergenic fungi in the documents repository environment of the National Archive of Cuba. Austin Journal of Public Health and Epidemiology, 5(3), 1077. https://austinpublishinggroup.com/public-health-epidemiology/fulltext/ajphe-v5-id1077.php.

[21] Viegas, C., Pinheiro, A.C., Sabino, R., et al., 2015. Environmental mycology in public health: Fungi and mycotoxins risk assessment and management, 1st ed.; Academic Press: Cambridge, Massachusetts, UK.

[22] Sánchis, J., 2002. Los nueve parámetros más críticos en el muestreo microbiológico del aire. Revista Técnicas de Laboratorio, 24(276), 858-862. https:// www.microkit.es/publicaciones/12-publi%20parametros%20criticos%20en%20control%20ambiental. pdf.

[23] Sánchez, K.C., Almaguer, M., Pérez, I., et al., 2019. Diversidad fúngica en la atmósfera de La Habana (Cuba) durante tres períodos poco lluviosos. Revista Internacional de Contaminación Ambiental. 35, 137- 150. DOI: http://dx.doi.org/10.20937/RICA.2019.35.01.10

[24] Barnett, H.L., Hunter, B.B., 1998. Illustrated genera of imperfect fungi, 4th ed.; APS Press: Minneapolis, USA.

[25] Domsch, K.H., Gams, W., Anders, T.H., (Eds.), 1980. Compendium of soil fungi. Academic Press LTD: London, UK.

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

[27] Pitt, J.I., 2000. A laboratory guide to common Penicillium species, 3rd ed.; Food Science Australia: Australia.

[28] Simões, M.F., Santos, C., Lima, N., 2013. Structural diversity of Aspergillus (section Nigri) spores. Microscopy and Microanalysis. 19(5), 1151-1158. DOI: https://doi.org/10.1017/S1431927613001712

[29] Samson, R.A., Noonim, P., Meijer, M., et al., 2007. Diagnostic tools to identify black aspergilla. Study in Mycology. 59, 129-145. DOI: https://doi.org/10.3114/sim.2007.59.13

[30] Visagie, C.M., Houbraken, J., Frisvad, J.C., et al., 2014. Identification and nomenclature of the genus Penicillium. Study in Mycology. 78, 343-371. DOI: https://doi.org/10.1016/j.simyco.2014.09.001

[31] Chen, A.J., Hubka, V., Frisvad, J.C., et al., 2017. Polyphasic taxonomy of Aspergillus section Aspergillus (formerly Eurotium), and its occurrence in indoor environments and food. Studies in Mycology. 88, 37- 135. DOI: https://doi.org/10.1016/j.simyco.2017.07.001

[32] Ellis, M.B., 1971. Dematiaceous hyphomycetes. Commonwealth Mycological Institute: England.

[33] Ellis, M.B., 1976. More Dematiaceous hyphomycetes. Commonwealth Mycological Institute: England.

[34] Bensch, K., Groenewald, J.Z., Dijksterhuis, J., et al., 2010. Species and ecological diversity within the Cladosporium cladosporioides complex (Davidiellaceae, Capnodiales). Studies in Mycology. 67, 1-94. DOI: https://doi.org/10.3114/sim.2010.67.01

[35] Bensch, K., Groenewald, J.Z., Meijer, M., et al.,2018. Cladosporium species in indoor environments. Studies in Mycology. 89, 177-301. DOI: https://doi.org/10.1016/j.simyco.2018.03.002

[36] Smith, G., 1980. Ecology and field biology. 2nd ed.; Harper & Row: New York, USA.

[37] Esquivel, P.P., Mangiaterra, M., Giusiano, G., et al., 2003. Microhongos anemófilos en ambientes abiertos de dos ciudades del nordeste argentino. Boletín Micológico. 18, 21-28. DOI: https://doi.org/10.22370/bolmicol.2003.18.0.376

[38] Moreno, C.E., 2001. Métodos para medir la biodiversidad. M&T-Manuales y Tesis SEA: Zaragoza, España.

[39] González OF, Arango ED, Moreno B, Leyva M, Berenguer Y. (2021). Comportamiento de la actividad sísmica anómala iniciada el 17 de enero de 2016 al sur de Santiago de Cuba. Minería y Geología, 37(2), 130-145. https://www.redalyc.org/journal/2235/223568255001/ html/.

[40] Weather Atlas, 2021. Previsión meteorológica y clima mensual Santiago de Cuba, Cuba. https://www. weather-atlas.com/es/cuba/santiago-de-cuba-clima.

[41] Karbowska-Berent, J., Górny, R.L., Strzelczyk, A.B., et al., 2011. Airborne and dust borne microorganisms in selected Polish libraries and archives. Building and Environment. 46, 1872-1879. DOI: https://doi.org/10.1016/j.buildenv.2011.03.007

[42] Yang, C., Pakpour, S., Klironomos, J., et al., 2016. Microfungi in indoor environments: What is known and what is not. In Biology of microfungi, fungal biology; Li, D-W., Ed.; Springer International Publishing: Switzerland. pp. 373-412. DOI: https://doi.org/10.1007/978-3-319-29137-6_15

[43] Pinheiro, A.C., 2014. Fungal communities in archives: Assessment strategies and impact on paper conservation and human health. PhD Thesis. Universidad de Nova de Lisboa: Portugal. https://run.unl.pt/ bitstream/10362/14890/1/Pinheiro_2014.pdf.

[44] Kalyoncu, F., 2010. Relationship between airborne fungal allergens and meteorological factors in Manisa City, Turkey. Environmental Monitoring and Assessment. 165, 553-558. DOI: https://doi.org/10.1007/s10661-009-0966-x

[45] Resolución No. 201. Lineamientos generales para la conservación de las fuentes documentales de la República de Cuba. Ministerio de Ciencia, Tecnología y Medio Ambiente (CITMA). Gaceta Oficial no. 55, Ordinaria de 2020, Cuba. https://www. gacetaoficial.gob.cu/es/gaceta-oficial-no-55-ordinaria-de-2020.

[46] Novohradská, S., Ferling, I., Hillmann, F., 2017. Exploring virulence determinants of filamentous fungal pathogens through interactions with soil amoebae. Frontiers in Cellular and Infection Microbiology. 7, 497. DOI: https://doi.org/10.3389/fcimb.2017.00497

[47] Díaz MJ, Gutiérrez A, González MC, Vidal G, Zaragoza RM, Calderón C. (2010). Caracterización aerobiológica de ambientes intramuro en presencia de cubiertas vegetales. Revista Internacional de Contaminación Ambiental, 26(4), 279-289. https://www. redalyc.org/pdf/370/37015993003.pdf.

[48] Elenjikamalil, S.M.R., Kelkar-Mane, V., 2019. Seasonal variations in the aerobiological parameters of a state archival repository in India. World Journal of Pharmaceutical Research. 8(5), 1459-1474. DOI: https://doi.org/10.20959/wjpr20195-14734

[49] Fekadu, S., Melaku, A., 2014. Microbiological quality of indoor air in university libraries. Asian Pacific Journal of Tropical Biomedicine. 4(Suppl 1), S312-S317. DOI: https://doi.org/10.12980/APJTB.4.2014C807

[50] Osman ME, Abdel Hameed AA, Ibrahim HY, Yousef F, Abo Elnasr AA, Saeed Y. (2017). Air microbial contamination and factors affecting its occurrence in certain book libraries in Egypt. Egyptian Journal of Botany, 57, 93-118. https://journals.ekb.eg/article_3328_c2a38d2c1a72028eee89d3fe9ae159cf.pdf.

[51] Rodríguez JC, Rodríguez B, Borrego SF. (2014). Evaluación de la calidad micológica ambiental del depósito de fondos documentales del Museo Nacional de la Música de Cuba en época de lluvia. AUGMDOMUS, 6, 123-146. https://revistas.unlp.edu.ar/ domus/article/view/867/1277.

[52] Borrego, S., Molina, A., Abrante, T., 2020. Sampling and characterization of the environmental fungi in the Provincial Historic Archive of Pinar del Río, Cuba. Journal of Biomedical Research & Environmental Sciences. 1(8), 404-420. DOI: https://dx.doi.org/10.37871/jbres1172

[53] Borrego S, Molina A, Castro M. (2021). Assessment of the airborne fungal communities in repositories of the Cuban Office of the Industrial Property: Their influence in the documentary heritage conservation and the personnel’s health. Revista Cubana de Ciencias Biológicas, 9(1), 1-18. http://www.rccb.uh.cu/index. php/RCCB/article/view/312/388.

[54] Leite-Jr, D.P., Pereira, R.S., Almeida, W.S., et al., 2018. Indoor air mycological survey and occupational exposure in libraries in Mato Grosso-Central Region-Brazil. Advances in Microbiology. 8, 324-353. DOI: https://doi.org/10.4236/aim.2018.84022

[55] Savković, Ž., Stupar, M., Unković, N., et al., 2021. Diversity and seasonal dynamics of culturable airborne fungi in a cultural heritage conservation facility. International Biodeterioration and Biodegradation. 157, 105-163. DOI: https://doi.org/10.1016/j.ibiod.2020.105163

[56] Mallo AC, Nitiu DS, Elíades LA, García M, Saparrat MCN. (2020). Análisis de la carga fúngica en el aire de la sala “Fragmentos de Historia a Orillas del Nilo” y del exterior del Museo de La Plata, Argentina. Ge-conservación, 17, 33-46. https://www.ge-iic.com/ojs/index.php/revista/article/ view/680/933.

[57] Pyrri, I., Tripyla, E., Zalachori, A., et al., 2020. Fungal contaminants of indoor air in the National Library of Greece. Aerobiologia. 36, 387-400. DOI: https://doi.org/10.1007/s10453-020-09640-0

[58] Stryjakowska-Sekulska M, Piotraszewska-Pająk A, Szyszka A, Nowicki M, Filipiak M. (2007). Microbiological quality of indoor air in University rooms. Polish Journal of Environmental Studies, 16(4), 623- 632. http://www.pjoes.com/Microbiological-Quality-of-Indoor-Air-r-nin-University-Rooms,88030,0,2. html.

[59] de Aquino Neto, F.R., de Goes Siqueira, L.F., 2000. Guidelines for indoor air quality in offices in Brazil. Proceedings of Healthy Buildings. 4, 549-554.

[60] Sabariego S, Díaz de la Guardia C, Sánchez FA. (2004). Estudio aerobiológico de los conidios de Alternaria y Cladosporium en la atmósfera de la ciudad de Almería (SE de España). Revista Iberoamericana de Micología, 21, 121-127. https://1library.co/document/y8pk5w5z-estudio-aerobiologico-de-los-conidios-de-alternaria-y-cladosporium-en-la-atmosfera-de-la-ciudad-de-almeria-se-de-espana.html.

[61] Borrego, S., Lavin, P., Perdomo, I., et al., 2012. Determination of indoor air quality in archives and the biodeterioration of the documentary heritage. ISRN Microbiology. DOI: https://doi.org/10.5402/2012/680598

[62] Almaguer M, Rojas TI. (2013). Aeromicota viable de la atmósfera de La Habana, Cuba. Nova Acta Científica Compostelana (Bioloxía), 20, 35-45. https:// revistas.usc.gal/index.php/nacc/article/view/1404.

[63] Kadaifciler, D.G., 2017. Bioaerosol assessment in the library of Istanbul University and fungal flora associated with paper deterioration. Aerobiologia. 33, 151- 166. DOI: https://doi.org/10.1007/s10453-016-9457-z

[64] Yang, C.S., Li, D.W., 2007. Ecology of fungi in the indoor environment. In Sampling and analysis of indoor microorganisms; Yang, CS., Heinsohn PA., Eds.; Jhon Wiley & Sons, Inc.: New Jersey, USA. pp. 191-214. DOI: https://doi.org/10.1002/9780470112434.ch10

[65] Cepeda, R., Luque, L., Ramírez, D., et al., 2019. Monitoreo de hongos ambientales en laboratorios y reservas patrimoniales bioarqueológicas. Boletín Micológico. 34(2), 33-49. DOI: http://dx.doi.org/10.22370/bolmicol.2019.34.2.1909

[66] Heredia, G., Arias-Mota, R.M., Mena-Portales, J., et al., 2018. Saprophytic synnematous microfungi. New records and known species for Mexico. Revista Mexicana de Biodiversidad. 89, 604-618. DOI: https://doi.org/10.22201/ib.20078706e.2018.3.2352

[67] Borrego S, Guiamet P, Vivar I, Battistoni P. (2018). Fungi involved in biodeterioration of documents in paper and effect on substrate. Acta Microscopica, 27, 37- 44. https://acta-microscopica.org/acta/article/ download/112/33.

[68] Karakasidou, K., Nikolouli, K., Amoutzias, G.D., et al., 2018. Microbial diversity in biodeteriorated Greek historical documents dating back to the 19th and 20th century: a case study. Microbiology Open. e596. DOI: https://doi.org/10.1002/mbo3.596

[69] Adelantado, C., Bello, C., Borrell, A., et al., 2005. Evaluation of the antifungal activity of products used for disinfecting documents on paper in archives. Restaurator. 26, 235-238. DOI: https://doi.org/10.1515/REST.2005.235

[70] Kraková, L., Šoltys, K., Otlewska, A., et al., 2018. Comparison of methods for identification of microbial communities in book collections: Culture-dependent (sequencing and MALDI-TOF MS) and culture-independent (IlluminaMiSeq). International Biodeterioration and Biodegradation. 131, 51-59. DOI: https://doi.org/10.1016/j.ibiod.2017.02.015

[71] Rojas, T.I., Aira, M.J., Batista, A., et al., 2012. Fungal biodeterioration in historic buildings of Havana (Cuba). Grana. 51, 44-51. DOI: https://doi.org/10.1080/00173134.2011.643920

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

[73] Almaguer M, Sánchez KC, Rojas TI. (2017). Dinámica de conidióforos de Zygosporium en la atmósfera de La Habana, Cuba. Revista Cubana de Ciencias Biológicas, 5, 1-7. http://www.rccb.uh.cu/index.php/ RCCB/article/view/189/299.

[74] Guild, S., MacDonald, M., 2004. Mould prevention and collection recovery: Guidelines for heritage collections. Technical Bulletin No 26. Canada: Canadian Conservation Institute (CCI). https://www.cci-icc. gc.ca/resources-ressources/publications/downloads/ technicalbulletins/eng/TB26-MouldPrevention.pdf.

[75] de Hoog, G.S., Guarro, G., Gene, J., et al., 2000. Atlas of clinical fungi, 2nd ed.; Centraalbureau voor Schimmelcultures (CBS): The Netherlands.

[76] Hedayati, M.T., Pasqualotto, A.C., Warn, P.A., et al., 2007. Aspergillus flavus: Human pathogen, allergen and mycotoxin producer. Microbiology. 153, 1677- 1692. DOI: https://doi.org/10.1099/mic.0.2007/007641-0

[77] Rudramurthy, S.M., Paul, R.A., Chakrabarti, A., et al., 2019. Invasive aspergillosis by Aspergillus flavus: Epidemiology, diagnosis, antifungal resistance, and management. Journal of Fungi. 5(3), 55. DOI: https://doi.org/10.3390/jof5030055

[78] de Hoog, G.S., Zalar, P., van den Ende, B.G., et al., 2005. Relation of halotolerance to human-pathogenicity in the fungal tree of life: An overview of ecology and evolution under stress. In Adaptation to life at high salt concentrations in archaea, bacteria, and eukarya; Gunde-Cimerman, N., Oren, A., Plemenitaš A. Eds.; Springer: The Netherlands. pp. 373-395.

[79] Pérez I, Sánchez KC. (2019). Aspectos fisiológicos del género Cladosporium desde la perspectiva de sus atributos patogénicos, fitopatogénicos y biodeteriorantes. Revista Cubana de Ciencias Biológicas, 7, 1-10. http://www.rccb.uh.cu/index.php/RCCB/article/view/255/331.

[80] Krijgsheld, P., Altelaar, A.M., Post, H., et al., 2012. Spatially resolving the secretome within the mycelium of the cell factory Aspergillus niger. Journal of Proteome Research. 11(5), 2807-2818. DOI: https://doi.org/10.1021/pr201157b

DOI: https://doi.org/10.30564/jasr.v5i2.4536


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