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Article

Biodeterioration Risk Assessment in Libraries by Airborne Fungal Spores

by
Yiniva Camargo-Caicedo
1,2,
Hilary Borja Pérez
2,
Maryann Muñoz Fuentes
2,
Eliana Vergara-Vásquez
1,2,* and
Andrés M. Vélez-Pereira
3,*
1
Programa de Ingeniería Ambiental y Sanitaria, Facultad de Ingeniería, Universidad del Magdalena, Santa Marta 470004, Colombia
2
Grupo de Investigación en Modelación de Sistemas Ambientales-GIMSA, Facultad de Ingeniería, Universidad del Magdalena, Santa Marta 470004, Colombia
3
Departamento de Ingeniería Mecánica, Facultad de Ingeniería, Universidad de Tarapacá, Arica 1000000, Chile
*
Authors to whom correspondence should be addressed.
J. Fungi 2024, 10(10), 680; https://doi.org/10.3390/jof10100680
Submission received: 7 September 2024 / Revised: 25 September 2024 / Accepted: 27 September 2024 / Published: 29 September 2024

Abstract

:
Fungal growth on cellulose-based materials in libraries can have detrimental effects on books and documents. This biodeterioration affects their physical, chemical, and esthetical characteristics. Thus, this work aimed to assess fungal aerosols’ concentrations and biodeterioration risk in two public libraries with artificial ventilation: the Banco de la República and CAJAMAG libraries. Air sampling was performed using a two-stage viable Andersen cascade impactor with Sabouraud dextrose agar at 4% on Petri dishes. Also, the temperature and relative humidity were measured with a digital thermo-hygrometer HOBO U12 Data Logger. The concentrations were low, with values of around 35 CFU/m3. Aspergillus, Cladosporium, and Penicillium were the predominant genera in the two libraries, with A. niger being the most abundant species. The thermo-hygrometric conditions inside the libraries were stable, with a mean temperature of 25.2 °C and a mean relative humidity of 52.1%. The calculated potential risk associated with fungal aerosols was seen to be medium in both libraries, where Aspergillus genera reported the highest cellulosic activity and hence had a higher risk of biodeterioration.

1. Introduction

Libraries and archives have been used for centuries to preserve various materials and store valuable information [1]. These documents which can have organic or synthetic compositions do deteriorate over time [2]. This is because these materials are potential nutrients [3] for microorganisms. Several factors can cause risks to materials and people’s health in libraries [4]. Biodeterioration is one of the main factors affecting long-term storage [5], where a complex phenomenon occurs along with other decomposition causes [6]. A prevention protocol by Polo et al. [7] requires the identification of microorganisms as a priority, particularly for both bacteria and fungi [8,9,10].
Fungi, unlike bacteria, are considered the most important organisms as biodeterioration agents of organic matter [11]. Likewise, they have been noted as the most frequent deterioration agents in historical libraries and archives [12]. Among the genera of fungi, the most frequently characterized biodeterioration agents are Aspergillus, Penicillium, Cladosporium, Chaetomium, Fusarium, Trichoderma, Alternaria, and Paecilomyces. These genera overlap with the airborne fungal spores in the library documented by Camargo-Caicedo et al. [13], where the most common ones are Aspergillus, Cladosporium, and Penicillium. Thus, airborne fungal spores’ concentration in libraries can indicate their presence in the collections, so it is possible to use them as an indirect indicator of the risk of deterioration [13,14].
Fungi causes chromatic alterations via the formation of stains of different colors, shades, and textures due to mycelial growth and pigment production. When they grow on paper, they degrade all the carbon-containing components, such as cellulose, and excrete organic acids deposited on the substrate [14,15,16]. Fungi produce different enzymes, such as cellulase, amylase, xylanase, and gelatinase; some of them are extracellular enzymes, which provoke the breakdown of paper components and could be accelerated by the growth of fungal hyphae [17,18]. The biodeterioration of books can be esthetic, color change [19], or reddish-brown spots [20], but also causes effects like paper weakness [21]. Aspergillus niger is the most common species reported with a high potential for the biodeterioration of paper books, showing a higher growth rate on cellulose substrate [22,23,24].
Additionally, airborne fungal spores in libraries are linked with health risks. Most of the previous genera mentioned, or their metabolites/proteins, have been reported as aeroallergens [25,26,27,28,29,30]. This could irritate the respiratory system, affecting the health of workers and visitors [31]. Such effects range from a mild allergy [32] to critical cases of aspergillosis or phaeohyphomycosis [33]. The main route of exposure is contact with the contaminated material [34]. It should be clarified that fungal infections can occur in any age group, but the symptoms differ according to the immunity status of the individual [35]. Fungi may behave as allergens, and if the concentration of spores is over 2.000 UFC/m3, they can be seen to elevate the risk factors for health [36].
The fungi grow at 63–100% relative humidity and between a 15 and 35 °C temperature [17]. This growth rate is higher when the temperature is above 23 °C and the relative humidity exceeds 65% [37]. When favorable microclimatic conditions are present, microorganisms are likely to infect library collections and initiate the process of their biodeterioration [38]; these actively growing organisms can form biofilms on surfaces in indoor environments and release spores into the air, dominating the site-specific microbiological community [7]. In addition to high temperature and humidity [1,14,39], other physical and chemical factors, such as dust [14,34] and poor air circulation [37], together with poor ventilation and inhomogeneity in the surface temperature of materials, can produce local water condensation points with a higher availability for fungi or bacteria than in the rest of an indoor environment [7].
Several studies have analyzed the microclimate within historic libraries, but comparisons are difficult because of the lack of long-term microclimatic observations and uniformity in the use of standards and risk assessment methods [40,41]. The methods for assessing the risk from biological agents include BIOGAVAL (Generalitat Valenciana), Osakidetza (Basque Country), classification by groups [42], and the standard operating procedure—PNO [43], among others. However, this methodology is focused on biological occupational risk. Currently, no methodology has been proposed for the biodeterioration of books.
In indoor environments, the biological component of air constitutes a potential element of degradation. Hence, the prompt and effective identification of biological aerosols and the thermo-climatic condition will also be relevant to assessing the collections’ risk conditions [14]. In this sense, this is the first work at the Banco de la República y CAJAMAG libraries in the District of Santa Marta, Colombia, that aimed to assess airborne fungal spores’ concentration and associated biodeterioration risk, identifying the genera and environmental conditions in two public libraries.

2. Materials and Methods

2.1. Study Area

This study was undertaken in two public libraries in the District of Santa Marta, Colombia: the Banco de la República and CAJAMAG libraries. The Banco de la República library has an area of 415.8 m2, with a bibliographic collection of more than 30,000 copies, and it has a general room made up of 45 open shelves with free access to the collection. It also has a reading room for newspapers and magazines (details in Figure 1). The CAJAMAG library has an area of 233.7 m2 and is furnished with seven open shelves, eight closed shelves serving as a newspaper library, and one closed archive area (details in Figure 2). These libraries have artificial ventilation systems by means of air conditioning devices distributed throughout the total available area.

2.2. Sampling

The air sampling was performed in five campaigns using a two-stage viable Andersen cascade impactor Model TE-10-860 (Tisch Environmental, village of Cleves, South Miami, OH, USA) for the collection of sedimentable viable particles (stage 1) and respirable viable particles (stage 6). The sample was collected into Petri dishes utilizing 4% Sabouraud dextrose agar (SDA) as a selective culture medium for isolating fungi (Figure S1). The equipment was positioned at a height of 1.5 m, and a flow rate of 28.3 l/min throughout the sampling was used, verified by an air rotameter connected to the pumping system of the impactor. The sample time was determined by preliminary sampling at three time intervals (4, 6, and 10 min) to determine the most efficient sampling practices. These intervals were based on the criteria indicated in previous studies [44,45,46,47]. The optimal time selected was four minutes according to the confidence limits and precision test results. Two monitoring points per library were established: Point 1 in the general room and Point 2 in the reading room. In both cases, the selection criteria used were the location of the collections and the influence of the mass air circulation of the air-conditioning systems. The samples were collected in duplicate (an original and a replica), and each monitoring session was carried out over 40-min intervals in the morning and afternoon. During the sampling inside the libraries, a digital thermo-hygrometer HOBO U12 Data Logger was used to measure the temperature (T, °C) and relative humidity (RH, %).
To ensure the quality of the measurements made in this study, a control protocol was applied for four processes associated with the preliminary steps, during and after monitoring: (1) agar preparation, (2) sampling dishes conditioning, (3) sterilization of the impactor between changing dishes using alcohol and thermal shock (flaming), and (4) control of samples’ incubation conditions (see Figure S2). Equally, other strategies were applied to guarantee the quality of the samples, such as the preparation of additional Petri dishes which were incubated at the end of each monitoring (control dishes) to verify the absence of growth of microorganisms. Similarly, another strategy involved sealing the dishes with paraffin film and wrapping them in plastic film to avoid the entry of particles, microorganisms, or any other external agent.

2.3. Sample Processing and Analysis

After the collection of the samples, the processing of these was carried out by incubation of the agar dishes for five days at 25 °C. Once the incubation was completed, the fungal colonies in the Petri dishes were counted to calculate the concentration expressed in colony-forming units per m3 (CFU m−3). This calculation was realized from the sum of the arithmetic average between the original and replica samples of each stage.
Fungal genera were identified through both macroscopic and microscopic analyses. In macroscopic identification, we register information about color, texture, and edge, among others; in the microscopic examination, each colony was transferred to slides, stained with lactophenol blue, and observed under 10X, 40X, and 100X objectives. The identification was based on fungal morphological characteristics (conidia, spores, and other resistance structures), following the taxonomic keys of Raper and Fennell [48] (1965), Barnett and Hunter [49], and Carrillo [50]. Genera were identified by strictly adhering to these morphological keys and corroborating the identifications using the MycoBank online database (https://www.mycobank.org/ accessed on 20 September 2024). This process was overseen by mycologist Leda Sotomayor (RIP).

2.4. Biodeterioration Risk Assessment

A simple methodology has been proposed to assess the potential biodeterioration risk on collections from airborne fungal spore concentrations. The risk calculation is based on the apparition frequency, concentration threshold, and potential biodeterioration of each genus/species. All these criteria were transformed into four categories: low (1), medium (2), high (4), and very high (5). The frequency and concentration thresholds will be established with quartiles from the dataset. In contrast, the potential of biodeterioration was established according to the literature, taking two criteria: (a) if the genus/species is recognized to degrade cellulose and (b) information about their degradation kinetic (if available). The equation to establish the risk is the sum of frequency and concentration thresholds multiplied by biodegradation potential, so the risk scale is between 2 and 50. A value between 2 and14 is low risk, 15 and 26 is medium risk, 27 and 38 is high risk, and 39 and 50 is very high risk.

2.5. Statistical Analysis

The samples from each library were analyzed separately, applying one-factor analysis of variance (ANOVA) to determine statistically significant differences between the fungal spore concentrations and each thermo-hygrometric condition (temperature or relative humidity). A multivariate regression was applied to determine the influence of the thermo-hygrometric conditions on the fungal spore concentrations, for which different models were evaluated to establish the best fit. The tests were conducted with a 95% interval confidence and a p-value of 0.05 using the statistical software Statgraphics version XVIII.

3. Results

3.1. Airborne Fungal Spores’ Concentration

Figure 3 shows the concentration of the fungal aerosols in the libraries under study. Higher maximum concentrations were seen in the CAJAMAG library in comparison with the Banco de la República library with maximum values of 300.4 CFU/m3, followed by 273.9 CFU/m3 and 247.3 CFU/m3, as noted during the morning period. This trend was also seen in the average concentrations, with the CAJAMAG library mean (35.7 CFU/m3) concentration being greater than that of the Banco de la República library (25.0 CFU/m3), but this difference was less stark than that seen for the maximum values. Likewise, in both study areas, the fungal aerosol concentration is greater in the morning than in the afternoon. Meanwhile, the sampling points in each library had generally tight distributions. The concentration through the campaigns is homogeneous, although the Banco de la República library is more variable than the CAJAMAG library. Despite this, the CAJAMAG library shows more peak concentrations, 90% of the time, and the concentration is below 90 CFU/m3.
Figure 4 shows the eleven fungal genera that were identified (only eight of these in the Banco de la República library and ten in the CAJAMAG library). Moreover, nine species of Aspergillus and one of Cunninghamella, Eurotium, and Paecilomyces were identified. Aspergillus is the genera most abundant in both libraries, followed by Cladosporium and Sterile mycelia in the Banco de la República library; and Penicillium and Cladosporium in the CAJAMAG library. Among all the identified species, Aspergillus niger (A. niger) is the most abundant. Finally, the most frequent genus/species is A. niger, followed by A. glaucus and Sterile mycelia, which is congruent with the genera/species with higher concentrations.

3.2. Thermo-Hygrometric Conditions

In the case of the thermo-hygrometric conditions, the results show 25.2 °C as the mean temperature and 52.1% as the mean RH. The temperature was homogeneous in both libraries, but the CAJAMAG library shows a slightly larger difference between the monitoring points, with higher temperature records in the morning than in the afternoon. The temperature varies more in the morning than in the afternoon, but to a greater degree in the Banco de la República library. In the case of RH, the values were more stable (with few changes) in the Banco de la República library and more varied in the CAJAMAG library. The behavior of the thermo-hygrometric conditions allows us to infer that the air mass in the libraries is generally homogeneous, with slightly more variability in the CAJAMAG library (Figure 5).

3.3. Statistical Results

The result of the statistical test is displayed in Table 1. The thermo-hygrometric conditions only show a slight influence in the CAJAMAG library, where RH strongly influences the airborne fungal spore concentration. However, the correlation in all cases is weak due to the R2 coefficient explaining only 14% of the observed variance, despite the high statistical significance of 95%. This can be corroborated in Figure 6, which shows the graphical correlation between the variables.

3.4. Biodeterioration Risk Assessment Results

Table 2 shows the results of the potential risk of biodeterioration associated with airborne fungal spore concentration in the libraries. In general, the potential risk is medium in both libraries. However, the afternoon has slightly higher values than the morning. The difference could be explained by the fact that morning has more diversity of fungi aerosols but a lower concentration than the afternoon, which shows less diversity but a high concentration. Of the fourteen genera/species identified, Aspergillus is the genus that is recognized as having a high potential for biodegradation according to the literature, where A. niger is mostly reported as having high cellulose activity.

4. Discussion

Biodeterioration is defined as a negative change in the properties of paper materials, wood, textiles, and other items of cultural heritage by the action of microorganisms, and it produces significant damage worldwide. Some fungi have the potential to destroy cellulose and lignin and disperse spores to extend their range [17]. The biological activity of biodeterioration is influenced by environmental factors, as has been mentioned. The temperature (fungi can grow between 10 and 40 °C), humidity (some species of fungi can survive between 60 and 80%), dust (supplies a nutritive layer for the fungi and the nucleus for the moisture), pH (fungi grow in acidic conditions between 5.5 and 6.0, except A. niger, which grows in pH 2), and atmospheric pollution [17] have all been seen to impact the concentrations and species present.
In addition to environmental factors, the concentration of fungi allows us to infer the risk or potential state of biodeterioration of the material. In the present study, the reported values are low, compared with another investigation summarized by Camargo Caicedo et al. [13], except for the research conducted by Savković et al. [51], who reported a concentration of over 25,000 CFU/m3 in a closed cultural heritage conservation facility. In this work, the documents were older and possibly not always stored in the best conditions.
If we compare it with another study in the same city, the values are again relatively low; the difference is attributed to the ventilation condition. The present results correspond to closed libraries with artificial ventilation, while the other studies utilized natural ventilation [13]. This is consistent within the study area; the Caribbean aerobiological studies suggest high fungal spore concentrations associated with a high temperature and RH [52,53,54,55]; such conditions should influence the concentration of the library with natural ventilation [3,9,56] to a greater extent than artificially ventilated ones. However, it is of note that for 90% of the time, the concentrations are below 90 CFU/m3, which implies a low or null risk of biodeterioration. This is consistent with Rodríguez et al. [10], who posited that concentrations above 100 CFU/m3 are indicative of risk to library collections.
Climate conditions can encourage the growth and adaptation of fungi, and in a suitable habitat, this can lead to the secretion of various active metabolites, such as enzymes and acids, as has been reported in previous works [17,20,57]. In addition, the efficacy of isolated fungal strains in producing a variety of enzymes is characterized by their ability to secrete acidic metabolites, as was reported previously [18]. In our case, the climate conditions in the libraries show stable values throughout the day, and this explains the low correlation values and significance between thermo-hygrometric conditions and airborne fungal spore concentration; at the same time, this could be evidence that indoor environmental conditions are good for collection conservation. This agrees with Ruga et al. [14], who state that low variability of temperature and RH values in indoor conditions could reduce the airborne fungal spore concentration. Equally, Gallo et al. [58] argue that air conditioning systems can regulate the thermo-hygrometric variables, so if such parameters are adequately controlled, there is no risk of biodeterioration.
Statistical investigations have revealed that the highest percentages of infection in libraries are due to Aspergillus (approximately 30%) and Penicillium (more than 30%), and that the parts of the books that are most attacked are the first and last pages, the outer margins, and the binding [58]. Likewise, previous studies carried out in the repositories of the National Archive of the Republic of Cuba [2] coincide with the main genera identified in the present study: Aspergillus, Cladosporium, and Penicillium. In addition, the species A. flavus, A. niger, A. terreus, A. versicolor, C. cladosporoides, C. elatum, C. fulvum, C. oxysporum, P. aurantiogroseum, P. commune, P. griseofulvum, and Mucor are known to have qualitative cellulosic activity, produce organic acids, and excrete pigments onto paper [2].
Another study carried out on paper documents from the 19th and 20th centuries stored in the National Archive of the Republic of Cuba and in Argentinean archives reported the predominant genera Aspergillus (A. flavus and A. niger species), Cladosporium, Fusarium, and Scopulariopsis, and in lower concentrations Eurotium, Paecilomyces, and Penicillium [57]. Again, this is consistent with the results of the present study, and with the genera that have been reported previously in other studies [15,59,60]. Also, the predominance of Aspergillus in various climatic zones is explained by the cosmopolitan nature of this genus, as reported in the literature [26].
In our case, the most frequent species of Aspergillus is A. Niger, which was the most reported in the biodeterioration of paper due to its high cellulolytic activity. It reached a concentration of over 100 CFU/m3 several times during the sampling campaign. This could be of concern and be grounds for a higher biodeterioration risk value. However, the overall assessment risk was calculated to be medium for both libraries. This highlights the importance of knowing the precise airborne fungal spore concentration in an environment with artificial ventilation (closed indoor environment) and that the sources of microorganisms are relevant for indoor environments. Thus, if we recognize that the bibliographic material is a suitable substrate for the growth of fungi, their airborne fungal spore concentration can indirectly measure their presence in the books and, therefore, validate the establishment of the risk from their measurements. In that sense, aerobiological sampling would turn out to be more practical than the development of surface microbiological monitoring, especially in libraries with an extensive collection. This premise is corroborated by Ruga et al. [14], who monitored with two techniques the presence of airborne fungal spores’ concentration in a gallery in Italy with artificial ventilation, and assessed the behavior of the concentrations at different levels and rooms. They reported that rooms with similar structures, influenced by the same air masses, showed a correlation in fungal concentrations. Conversely, rooms that were not similar in this regard had a statistically different fungal concentration.
The biodeterioration of paper in books and documents depends on the enzymatic activity of microorganisms, so the intensity of fungi growth and the resultant damage is established by the fiber content in the paper and the type of glue used. The appearance of fungi in bibliographic material is associated with cellulolytic enzymes. Therefore, observations made by Strzelczyk and Leznicka [59] indicate that fungi are characterized by the active degradation of cellulose (i.e., the appearance of red stains on the edges and surface of the paper caused by the growth of Penicillium), as well as the formation of viscous substances.
No study is without its limitations, and this study is no different. Hence, there is a need to evaluate the methodology proposed here and to contrast the concentrations of the taxa identified in the bibliographic material and that of the airborne concentrations. This would greatly aid in precision, in terms of understanding the risk of biodeterioration. Future studies should include data on library use/users, activities, or mechanical movements that, in addition to the thermo-hygrometric conditions, potentially contribute to the release of fungal spores to evaluate the calculated risks.

5. Conclusions

The assessment of the biodeterioration risk caused by airborne fungal spores in two public libraries in the District of Santa Marta revealed that the CAJAMG library had the highest concentrations of fungi, reaching up to 300 CFU/m3. The average thermo-hygrometric conditions in both libraries are similar (25 °C, 50% RH), as well as the variability of the identified fungal genera. The most abundant species is Aspergillus niger, which is concerning due to its high potential for paper biodeterioration, posing a significant risk to the collections. Under the indicated environmental conditions, the potential risk of biodeterioration associated with the airborne fungal spore concentration in both libraries is medium.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/jof10100680/s1, Figure S1. Cascade impactor viable diagram, its relationship to aerodynamic particle size and the human respiratory system; Figure S2. The protocol for quality assurance and control in samples.

Author Contributions

Y.C.-C.: Conceptualization, Methodology, Discussion of the results, Writing—original draft preparation. H.B.P.: Visualization, Investigation. M.M.F.: Visualization, Investigation. E.V.-V.: Discussion of the results, Writing—reviewing and editing. A.M.V.-P.: Methodology, Data curation, Statistical analysis, Graphic representation, Discussion of the results, Writing—original draft preparation. All authors have read and agreed to the published version of the manuscript.

Funding

The research was funded by Universidad del Magdalena under Grant Agreement No. CFP-PCTeI 12–09, and Universidad de Tarapacá Grant No. UTA-MAYOR 5859-23.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data available on request.

Acknowledgments

The authors thank Universidad del Magdalena for supporting the project that led to this work and to the staff of the Banco de la República library and CAJAMAG library for their collaboration during the sampling. We also express gratitude to Engineer Leda Mendoza (RIP) for her valuable contributions in the identification of fungi aerosols. Finally, the authors thank Sheimy Lozano and Aldair Valle for their collaboration in drawing up the plans of the libraries. We appreciate the English proofreading of David O’Connor.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Cappitelli, F.; Fermo, P.; Vecchi, R.; Piazzalunga, A.; Valli, G.; Zanardini, E.; Sorlini, C. Chemical–Physical and Microbiological Measurements for Indoor Air Quality Assessment at the Ca’ Granda Historical Archive, Milan (Italy). Water Air Soil Pollut. 2009, 201, 109–120. [Google Scholar] [CrossRef]
  2. Borrego Alonso, S.; Perdomo Amistad, I. Caracterización de la micobiota aérea en dos depósitos del Archivo Nacional de la República de Cuba. Rev. Iberoam. Micol. 2014, 31, 182–187. [Google Scholar] [CrossRef]
  3. Savoldelli, S.; Cattò, C.; Villa, F.; Saracchi, M.; Troiano, F.; Cortesi, P.; Cappitelli, F. Biological Risk Assessment in the History and Historical Documentation Library of the University of Milan. Sci. Total Environ. 2021, 790, 148204. [Google Scholar] [CrossRef] [PubMed]
  4. Peña, L.M.; Reyes, G.A.P. Estudio de los factores de riesgos asociados a una biblioteca especializada en el Estado Lara, Venezuela. Biblios 2016, 64, 60–68. [Google Scholar] [CrossRef]
  5. Zhang, M.; Hu, Y.; Liu, J.; Pei, Y.; Tang, K.; Lei, Y. Biodeterioration of Collagen-Based Cultural Relics: A Review. Fungal Biol. Rev. 2022, 39, 46–59. [Google Scholar] [CrossRef]
  6. Konsa, K.; Tirrul, I.; Hermann, A. Wooden Objects in Museums: Managing Biodeterioration Situation. Int. Biodeterior. Biodegrad. 2014, 86, 165–170. [Google Scholar] [CrossRef]
  7. Polo, A.; Cappitelli, F.; Villa, F.; Pinzari, F. Biological Invasion in the Indoor Environment: The Spread of Eurotium Halophilicum on Library Materials. Int. Biodeterior. Biodegrad. 2017, 118, 34–44. [Google Scholar] [CrossRef]
  8. Branysova, T.; Demnerova, K.; Durovic, M.; Stiborova, H. Microbial Biodeterioration of Cultural Heritage and Identification of the Active Agents over the Last Two Decades. J. Cult. Herit. 2022, 55, 245–260. [Google Scholar] [CrossRef]
  9. Hassan, A.; Zeeshan, M.; Bhatti, M.F. Indoor and Outdoor Microbiological Air Quality in Naturally and Mechanically Ventilated University Libraries. Atmos. Pollut. Res. 2021, 12, 101136. [Google Scholar] [CrossRef]
  10. Rodriguez, J.C.R.; Rodriguez, B.R.; Borrego, S.F.B. Evaluación de la calidad micológica ambiental para la conservación de los fondos documentales del Museo Nacional de la Música de Cuba en época de lluvia. Augmdomus 2014, 6, 123–146. [Google Scholar]
  11. Bergaglio, C.; Pené, M. Conservación Preventiva en Archivos y Bibliotecas; Instituto Cultural de la Provincia de Buenos Aires, Dirección Provincial de Patrimonio Cultural, Archivo Histórico: La Plata, Argentina, 2009; ISBN 978-987-1245-58-1.
  12. Montanari, M.; Melloni, V.; Pinzari, F.; Innocenti, G. Fungal Biodeterioration of Historical Library Materials Stored in Compactus Movable Shelves. Int. Biodeterior. Biodegrad. 2012, 75, 83–88. [Google Scholar] [CrossRef]
  13. Camargo Caicedo, Y.; Borja Pérez, H.; Muñoz Fuentes, M.; Vergara-Vásquez, E.; Vélez-Pereira, A.M. Assessment of Fungal Aerosols in a Public Library with Natural Ventilation. Aerobiologia 2023, 39, 37–50. [Google Scholar] [CrossRef]
  14. Ruga, L.; Orlandi, F.; Fornaciari, M. Viable and Not Viable Spore Concentrations in National Gallery of Umbria (Italy). Aerobiologia 2021, 37, 363–372. [Google Scholar] [CrossRef]
  15. Ali, E.A.M.; Abdel-rahman, T.; Ali, D.M.I.; El-Badawey, N.F.; Fadel, M.S. Deterioration of Different Paper Types by Fungi Isolated from Cairo University’s Old Library. Egypt. J. Chem. 2022, 65, 467–482. [Google Scholar] [CrossRef]
  16. 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. Biodeterior. Biodegrad. 2010, 64, 139–145. [Google Scholar] [CrossRef]
  17. Koul, B.; Upadhyay, H. Fungi-Mediated Biodeterioration of Household Materials, Libraries, Cultural Heritage and Its Control. In Fungi and Their Role in Sustainable Development: Current Perspectives; Gehlot, P., Singh, J., Eds.; Springer: Singapore, 2018; pp. 597–615. ISBN 9789811303937. [Google Scholar]
  18. Fouda, A.; Abdel-Nasser, M.; Khalil, A.M.A.; Hassan, S.E.-D.; Abdel-Maksoud, G. Investigate the Role of Fungal Communities Associated with a Historical Manuscript from the 17th Century in Biodegradation. Npj Mater. Degrad. 2022, 6, 88. [Google Scholar] [CrossRef]
  19. Zotti, M.; Ferroni, A.; Calvini, P. Mycological and FTIR Analysis of Biotic Foxing on Paper Substrates. Int. Biodeterior. Biodegrad. 2011, 65, 569–578. [Google Scholar] [CrossRef]
  20. 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. Int. Sch. Res. Not. 2012, 2012, 680598. [Google Scholar] [CrossRef]
  21. Gutarowska, B.; Skora, J.; Zduniak, K.; Rembisz, D. Analysis of the Sensitivity of Microorganisms Contaminating Museums and Archives to Silver Nanoparticles. Int. Biodeterior. Biodegrad. 2012, 68, 7–17. [Google Scholar] [CrossRef]
  22. Fouda, A.; Abdel-Maksoud, G.; Abdel-Rahman, M.A.; Eid, A.M.; Barghoth, M.G.; El-Sadany, M.A.-H. Monitoring the Effect of Biosynthesized Nanoparticles against Biodeterioration of Cellulose-Based Materials by Aspergillus Niger. Cellulose 2019, 26, 6583–6597. [Google Scholar] [CrossRef]
  23. Naji, K.M.; Abdullah, Q.Y.M.; AL-Zaqri, A.Q.M.; Alghalibi, S.M. Evaluating the Biodeterioration Enzymatic Activities of Fungal Contamination Isolated from Some Ancient Yemeni Mummies Preserved in the National Museum. Biochem. Res. Int. 2014, 2014, e481508. [Google Scholar] [CrossRef] [PubMed]
  24. Romero, S.M.; Giudicessi, S.L.; Vitale, R.G. Is the Fungus Aspergillus a Threat to Cultural Heritage? J. Cult. Herit. 2021, 51, 107–124. [Google Scholar] [CrossRef]
  25. Vélez-Pereira, A.M.; De Linares, C.; Belmonte, J. Aerobiological Modeling I: A Review of Predictive Models. Sci. Total Environ. 2021, 795, 148783. [Google Scholar] [CrossRef]
  26. Vélez-Pereira, A.M.; De Linares, C.; Canela, M.; Belmonte, J. Spatial Distribution of Fungi from the Analysis of Aerobiological Data with a Gamma Function. Aerobiologia 2021, 37, 461–477. [Google Scholar] [CrossRef]
  27. Vélez-Pereira, A.M.; De Linares, C.; Canela, M.A.; Belmonte, J. A Comparison of Models for the Forecast of Daily Concentration Thresholds of Airborne Fungal Spores. Atmosphere 2023, 14, 1016. [Google Scholar] [CrossRef]
  28. De Linares, C.; Navarro, D.; Puigdemunt, R.; Belmonte, J. Airborne Alt a 1 Dynamic and Its Relationship with the Airborne Dynamics of Alternaria Conidia and Pleosporales Spores. J. Fungi 2022, 8, 125. [Google Scholar] [CrossRef] [PubMed]
  29. De Linares, C.; Navarro, D.; Puigdemunt, R.; Belmonte, J. Aspergillus Conidia and Allergens in Outdoor Environment: A Health Hazard? J. Fungi 2023, 9, 624. [Google Scholar] [CrossRef]
  30. Vitte, J.; Michel, M.; Malinovschi, A.; Caminati, M.; Odebode, A.; Annesi-Maesano, I.; Caimmi, D.P.; Cassagne, C.; Demoly, P.; Heffler, E.; et al. Fungal Exposome, Human Health, and Unmet Needs: A 2022 Update with Special Focus on Allergy. Allergy 2022, 77, 3199–3216. [Google Scholar] [CrossRef]
  31. Borrego, S. La bioseguridad en los archivos cubanos y la COVID-19. Bibl. Univ. 2020, 23, 246–261. [Google Scholar] [CrossRef]
  32. Fouda, A.; Abdel-Maksoud, G.; Abdel-Rahman, M.A.; Salem, S.S.; Hassan, S.E.-D.; El-Sadany, M.A.-H. Eco-Friendly Approach Utilizing Green Synthesized Nanoparticles for Paper Conservation against Microbes Involved in Biodeterioration of Archaeological Manuscript. Int. Biodeterior. Biodegrad. 2019, 142, 160–169. [Google Scholar] [CrossRef]
  33. Ferrándiz-Pulido, C.; Martin-Gomez, M.T.; Repiso, T.; Juárez-Dobjanschi, C.; Ferrer, B.; López-Lerma, I.; Aparicio, G.; González-Cruz, C.; Moreso, F.; Roman, A.; et al. Cutaneous Infections by Dematiaceous Opportunistic Fungi: Diagnosis and Management in 11 Solid Organ Transplant Recipients. Mycoses 2019, 62, 121–127. [Google Scholar] [CrossRef]
  34. Carrera, R.M.; Paladínez, R.C. Estudio de las condiciones de trabajo en bibliotecas de la ciudad de Quito y la exposición de sus trabajadores a hongos. Enfoque UTE 2017, 8, 94–106. [Google Scholar] [CrossRef]
  35. Suresh, S.; Arumugam, D.; Zacharias, G.; Palaninathan, S.; Vishwanathan, R.; Venkatraman, V. Prevalence and Clinical Profile of Fungal Rhinosinusitis. Allergy Rhinol. 2016, 7, ar.2016. [Google Scholar] [CrossRef]
  36. Moctezuma, M.; Domínguez, E.; Mateos, P.; Rodríguez, I.; Cárdenas, J.; Fragoso, L. Aislamiento de Hongos Alergenos En Una Biblioteca Universitaria. Acta Univ. 2015, 25, 32–38. [Google Scholar] [CrossRef]
  37. Delgado, K.L.A.; Díaz, A.G.; Palomino, D.R.; Aguilera, B. Factores Que Afectan El Fondo Bibliográfico de La Biblioteca de La Filial de Ciencias Médicas Mario Muñoz Monroy. Las Tunas. Innovación Tecnológica 2020, 26, 1–11. [Google Scholar]
  38. Kalwasinska, A.; Burkowska, A.; Wilk, I. Microbial Air Contamination in Indoor Environment of a University Library. Ann. Agric. Environ. Med. 2012, 19, 1. [Google Scholar]
  39. Toloza Moreno, D.L.; Lizarazo Forero, L.M. Aeromicrobiología Del Archivo Central De La Universidad Pedagógica y Tecnológica de Colombia (Tunja-Boyacá). Acta Biológica Colomb. 2011, 16, 185–194. [Google Scholar]
  40. Contreras, Z.R.; Ramirez Leal, P.; Contreras Velásquez, Z.R.; Ramirez Leal, P. Comparación de Métodos Utilizados en la Valoracion del Riesgo Biológico. Rev. Asoc. Española Espec. Med. Trab. 2019, 28, 91–108. [Google Scholar]
  41. Verticchio, E.; Frasca, F.; Bertolin, C.; Siani, A.M. Climate-Induced Risk for the Preservation of Paper Collections: Comparative Study among Three Historic Libraries in Italy. Build. Environ. 2021, 206, 108394. [Google Scholar] [CrossRef]
  42. Gallego, R. Evaluación simplificada de agentes biológicos en el trabajo. Rev. Enfermería Trab. 2011, 1, 102–107. [Google Scholar]
  43. Valdes, D.C.; Martínez, J.I.V.; Borges, M.C.C.; Guedes, A.R.; Ávila, Y.R.; Bazán, M.B.M. Metodología para la evaluación del riesgo biológico. Cienc. Holguín 2009, XV, 1–8. [Google Scholar]
  44. Grinshpun, S.A.; Buttner, M.P.; Mainelis, G.; Willeke, K. Sampling for Airborne Microorganisms. In Manual of Environmental Microbiology; John Wiley & Sons, Ltd.: Hoboken, NJ, USA, 2016; pp. 3.2.2-1–3.2.2-17. ISBN 978-1-68367-074-2. [Google Scholar]
  45. Vélez-Pereira, A.; Caicedo, Y.C.; Rincones, S.R.B. Distribución espacio-temporal de aerobacterias en el relleno sanitario Palangana, Santa Marta (Colombia). Intropica 2010, 5, 5–18. [Google Scholar]
  46. Vélez-Pereira, A.M.; Camargo Caicedo, Y. Aerobacterias en las unidades de cuidado intensivo del Hospital Universitario “Fernando Troconis”, Colombia. Rev. Cub Salud Pública 2014, 40, 362–368. [Google Scholar]
  47. Vélez-Pereira, A.M.; Camargo Caicedo, Y. Análisis de los factores ambientales y ocupacionales en la concentración de aerobacterias en unidades de cuidado intensivo del Hospital Universitario Fernando Troconis, 2009 Santa Marta-Colombia. Rev Cuid. 2014, 5, 595–605. [Google Scholar] [CrossRef]
  48. Raper, K.B.; Fennell, D.I. The Genus Aspergillus; Williams & Wilkins: Philadelphia, PA, USA, 1965; ISBN 978-0-88275-109-2. [Google Scholar]
  49. Barnett, H.L.; Hunter, B.B. Illustrated Genera of Imperfect Fungi; Macmillan: New York, NY, USA, 1987; ISBN 978-0-02-306395-4. [Google Scholar]
  50. Carrillo, L. Los Hongos de Los Alimentos y Forrajes. Univ. Nac. Salta Argent. 2003, 118, 20. [Google Scholar]
  51. Savković, Ž.; Stupar, M.; Unković, N.; Ivanović, Ž.; Blagojević, J.; Popović, S.; Vukojević, J.; Grbić, M.L. Diversity and Seasonal Dynamics of Culturable Airborne Fungi in a Cultural Heritage Conservation Facility. Int. Biodeterior. Biodegrad. 2021, 157, 105163. [Google Scholar] [CrossRef]
  52. Quintero, E.; Rivera-Mariani, F.; Bolaños-Rosero, B. Analysis of Environmental Factors and Their Effects on Fungal Spores in the Atmosphere of a Tropical Urban Area (San Juan, Puerto Rico). Aerobiologia 2010, 26, 113–124. [Google Scholar] [CrossRef]
  53. Almaguer, M.; Aira, M.-J.; Rodríguez-Rajo, F.-J.; Rojas, T.-I. Study of Airborne Fungus Spores by Viable and Non-Viable Methods in Havana, Cuba. Grana 2013, 52, 289–298. [Google Scholar] [CrossRef]
  54. Almaguer, M.; Díaz, L.; Fernández-González, M.; Valdéz, E. Allergenic Fungal Spores and Hyphal Fragments in the Aerosol of Havana, Cuba. Aerobiologia 2020, 36, 441–448. [Google Scholar] [CrossRef]
  55. Rivera-Mariani, F.E.; Almaguer, M.; Aira, M.J.; Bolaños-Rosero, B. Comparison of Atmospheric Fungal Spore Concentrations between Two Main Cities in the Caribbean Basin. Puerto Rico Health Sci. J. 2020, 39, 235–242. [Google Scholar]
  56. Okpalanozie, O.E.; Adebusoye, S.A.; Troiano, F.; Cattò, C.; Ilori, M.O.; Cappitelli, F. Assessment of Indoor Air Environment of a Nigerian Museum Library and Its Biodeteriorated Books Using Culture-Dependent and –Independent Techniques. Int. Biodeterior. Biodegrad. 2018, 132, 139–149. [Google Scholar] [CrossRef]
  57. Borrego, S.; Guiamet, P.; Vivar, I.; Battistoni, P. Fungi Involved in Biodeterioration of Documents in Paper and Effect on Substrate. Acta Microsc. 2018, 27, 37–44. [Google Scholar]
  58. Gallo, F.; Pasquariello, G.; Valenti, P. Libraries and Archives. In Cultural Heritage and Aerobiology: Methods and Measurement Techniques for Biodeterioration Monitoring; Mandrioli, P., Caneva, G., Sabbioni, C., Eds.; Springer: Dordrecht, The Netherlands, 2003; pp. 175–193. ISBN 978-94-017-0185-3. [Google Scholar]
  59. Strzelczyk, A.B.; Leznicka, S. The Role of Fungi and Bacteria in the Consolidation of Books. Int. Biodeterior. Bull. 1981, 17, 57–67. [Google Scholar]
  60. Nyuksha, Y.P. Some Special Gases of Biological Deterioration of Books. Resturator 1983, 5, 177–182. [Google Scholar]
Figure 1. Diagram of the Banco de la República library and detail on the bookshelf.
Figure 1. Diagram of the Banco de la República library and detail on the bookshelf.
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Figure 2. Diagram of the CAJAMAG library and detail on the bookshelf.
Figure 2. Diagram of the CAJAMAG library and detail on the bookshelf.
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Figure 3. The concentration of airborne fungal spores by library, the time of the day, and sampling point. * Extreme value is 1.5 times more than the 75th percentile. + Extreme value is three times more than the 75th percentile.
Figure 3. The concentration of airborne fungal spores by library, the time of the day, and sampling point. * Extreme value is 1.5 times more than the 75th percentile. + Extreme value is three times more than the 75th percentile.
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Figure 4. Percentage distribution of genera/species of fungi identified by library, the time of the day, and sampling point.
Figure 4. Percentage distribution of genera/species of fungi identified by library, the time of the day, and sampling point.
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Figure 5. Thermo-hygrometric conditions in libraries. The left side is temperature. The right side is relative humidity. At the top is the Banco de la República library, and at the bottom is the CAJAMAG library. * Extreme value is 1.5 times more than the 75th percentile.
Figure 5. Thermo-hygrometric conditions in libraries. The left side is temperature. The right side is relative humidity. At the top is the Banco de la República library, and at the bottom is the CAJAMAG library. * Extreme value is 1.5 times more than the 75th percentile.
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Figure 6. Correlation between thermo-hygrometric condition and airborne fungal spores’ concentration.
Figure 6. Correlation between thermo-hygrometric condition and airborne fungal spores’ concentration.
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Table 1. Statistical regression results regarding airborne fungal spores in the libraries.
Table 1. Statistical regression results regarding airborne fungal spores in the libraries.
LibraryParameterVariables in the Model
TemperatureRelative HumidityAll
Banco de la RepúblicaEquation y = 5.9 2.8 · 10 2 x 1 2 2 y = 3.0 + 54.21 x 2 2 y = 35.18 0.34 x 1 2.78 · 10 2   x 2
R20.67%0.30%0.04%
p-Value0.3190.5030.950
CAJAMAGEquation y = 69.8 + 0.15 x 1 2 y = 62.5 + 3.6 · 10 2 x 2 2 y = 181.28 + 2.73 x 1 + 2.91 x 2
R212.59%14.51%14.13%
p-Value0.0000.0020.000
y : Concentration of fungal spore, x 1 : temperature, x 2 : relative humidity. P-critic: 0.005, if the p-value < P-critic, there is statistical significance with the 95% level.
Table 2. Potential risk assessment of biodeterioration per library and genera of airborne fungal spores.
Table 2. Potential risk assessment of biodeterioration per library and genera of airborne fungal spores.
Banco de la República LibraryCAJAMAG Library
MorningAfternoonMorningAfternoon
Genera/SpecieBPFreqCTRiskFreqCTRiskFreqCTRiskFreqCTRisk
Aspergillus55550555055505550
A. cremeus52220222044401110
A. candidus1 0112112112
A. flavus54440454545454545
A. fumigatus544404440 0 0
A. glaucus45436543655405540
A. niger55550555045455550
A. ochraceus52220243022204545
A. terreus5 011101215 0
A. versicolor411811822164432
Chrysonilia1224 0123224
Cladosporium45540554045364536
Cunninghamella4118 0118118
C. matruchotii4 0 0118 0
Curvularia245184416114126
Eurotium4 0 0 0118
E. chevalieri4 0 0 0118
Geotrichum2 0 0 0114
Mucor2126 0 0 0
Paecilomyces4118 0 0 0
P. niveus4 0 02216 0
Penicillium441204 055405540
Sterile mycelia144855105510459
Torula2 0 0126 0
Yeast12242455510448
Global riskMedium (22)Medium (26)Medium (19)Medium (23)
BP: biodeterioration potential. Freq: frequency. CT: concentration thresholds. Red shading: very high risk. Orange shading: high risk. Green shading: medium risk. Blue shading: low risk.
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MDPI and ACS Style

Camargo-Caicedo, Y.; Borja Pérez, H.; Muñoz Fuentes, M.; Vergara-Vásquez, E.; Vélez-Pereira, A.M. Biodeterioration Risk Assessment in Libraries by Airborne Fungal Spores. J. Fungi 2024, 10, 680. https://doi.org/10.3390/jof10100680

AMA Style

Camargo-Caicedo Y, Borja Pérez H, Muñoz Fuentes M, Vergara-Vásquez E, Vélez-Pereira AM. Biodeterioration Risk Assessment in Libraries by Airborne Fungal Spores. Journal of Fungi. 2024; 10(10):680. https://doi.org/10.3390/jof10100680

Chicago/Turabian Style

Camargo-Caicedo, Yiniva, Hilary Borja Pérez, Maryann Muñoz Fuentes, Eliana Vergara-Vásquez, and Andrés M. Vélez-Pereira. 2024. "Biodeterioration Risk Assessment in Libraries by Airborne Fungal Spores" Journal of Fungi 10, no. 10: 680. https://doi.org/10.3390/jof10100680

APA Style

Camargo-Caicedo, Y., Borja Pérez, H., Muñoz Fuentes, M., Vergara-Vásquez, E., & Vélez-Pereira, A. M. (2024). Biodeterioration Risk Assessment in Libraries by Airborne Fungal Spores. Journal of Fungi, 10(10), 680. https://doi.org/10.3390/jof10100680

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