10.6092/issn.2531-7342/15988
Cultural heritage artefacts, such as stone works, books, manuscripts, and parchments, are subjected to severe biodeterioration processes over time caused by fungi, algae, lichens, and complex communities of microbial biofilms. Fungal contaminations are widespread as active or dormant spores which are present in the air and on objects and can lead to irreversible biodeterioration processes. Highly toxic and hardly biodegradable compounds are commonly used in cultural heritage conservation and restoration practices, which can be harmful even to the treated materials. Therefore, sector operators may be exposed to both biological and chemical risks, and often the failure to use adequate protective equipment increases the exposure risk. The interest of many researchers has been recently orienting, in this sector also, towards the use of natural products, as a valid alternative both for operators' health and environmental protection. This review aims to provide an overview of the biological and chemical risks associated with the treatment of fungal biodeterioration of artistic works and suggests the use of natural substances as a possible alternative to chemical synthetic products for the safety of restoration operators.
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Giovanni Pacioni
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Zammit G, Sánchez-Moral S, Albertano P (2011) Bacterially mediated mineralisation processes lead to biodeterirarion of artwork in Maltese catacombs. Science of the Total Environment 409:2773‒2782. https://doi.org/10.1016/j.scitotenv.2011.03.008
Natural substances as biocides in the fungi treatment on artistic products to protect the environment and health of restoration workers
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                IJM - Italian Journal of Mycology
                ISSN 2531-7342 - Vol. 52 (2023): 89-111
                Journal homepage: https://italianmycology.unibo.it/

Review

            Natural substances as biocides in the fungi treatment
             on artistic products to protect the environment and
                         health of restoration workers

          Laura Casorri1, Eva Masciarelli1, Barbara Ficociello1, Federica Ietto1,
        Federica Incoronato1, Marco Di Luigi2, Claudio Beni3, Giovanni Pacioni4
1
  Department of Technological Innovations and safety of plants, products and anthropic settlements (DIT) - National
Institute for Insurance against Accidents at Work - Via R. Ferruzzi, 38/40 - 00143 Rome, Italy.
2
  Department of Occupational and Environmental Medicine, Epidemiology and Hygiene (DiMEILA), National Institute
for Insurance against Accidents at Work,Via di Fontana Candida 1, 00078 Monte Porzio Catone - Rome, Italy.
3
  Council for Agricultural Research and Economics, Research Centre for Engineering and Agro-Food Processing, Via
della Pascolare 16, Monterotondo, 00015, Italy.
4
  Department of Life, Health and Environmental Sciences - MeSVA, University of L’Aquila, Coppito 1, 67100, L’Aquila,
Italy.

Corresponding author e-mail: m.diluigi@inail.it


Article info
Received 12/12/2022; accepted 17/4/2023
https://doi.org/10.6092/issn.2531-7342/15988

Abstract
Cultural heritage artefacts, such as stone works, books, manuscripts, and parchments, are subjected to severe
biodeterioration processes over time caused by fungi, algae, lichens, and complex communities of microbial
biofilms. Fungal contaminations are widespread as active or dormant spores which are present in the air and
on objects and can lead to irreversible biodeterioration processes. Highly toxic and hardly biodegradable
compounds are commonly used in cultural heritage conservation and restoration practices, which can be
harmful even to the treated materials. Therefore, sector operators may be exposed to both biological and
chemical risks, and often the failure to use adequate protective equipment increases the exposure risk. The
interest of many researchers has been recently orienting, in this sector also, towards the use of natural products,
as a valid alternative both for operators’ health and environmental protection. This review aims to provide
an overview of the biological and chemical risks associated with the treatment of fungal biodeterioration
of artistic works and suggests the use of natural substances as a possible alternative to chemical synthetic
products for the safety of restoration operators.

Keywords
cultural heritage, biodeterioration, biodeteriogens, biological risk, essential oil, hydrolates, plant extracts


Introduction

Cultural heritage is the complex set of material testimonies (artistic or symbolic) inherited from
previous generations, belonging not only to individual cultures but to all humanity (Jokilehto, 2005).
Over time, cultural heritage undergoes several biodeterioration processes triggered by the growth of
fungi (yeasts, mycelia, and molds), algae, lichens, and complex biofilms of microbial communities
Department of Agricultural and Food Science in partnership with the Italian Mycological Society (UMI).
The journal is hosted and maintained by ABIS-AlmaDL. © 2023 The Authors. This work is licensed under CC BY 4.0
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which represent an important aspect in the biodegradation processes of stone works and also of books,
manuscripts, and parchments. Biodeterioration can be defined as “any undesirable change in the
properties of a material caused by the vital activities of organisms” (Hueck, 2001). Contamination by
fungi, which are known to be important bio-deteriogens, is a common phenomenon, especially when
effective microclimatic control systems are lacking. Spores, whether active or dormant, are ubiquitous
in the air and on object surfaces, and they are the source of numerous biodeterioration processes,
which are often irreversible (Urzì and De Leo, 2010). These contaminations can spread quickly and
invasively with high humidity and poor ventilation or if extraordinary events occur (floods, pipes
ruptures, percolations, or air conditioning systems failures). These conditions could favor the massive
development of fungi harmful for the conservation of artistic heritage and for human health (Saifeldin
et al., 2014).
    In the restoration and protection activities of cultural heritage from fungi, highly toxic and non-
biodegradable compounds are commonly used, which are sometimes also harmful to the treated
materials. Consequently, the sector operators could be exposed both to biological and chemical risks
due respectively to pathogenic fungi and to chemical synthetic biocides. Furthermore, failure to use
adequate protective equipment could increase the exposure risk (D’Angelo et al., 2012). In many
fields, such as medical, industrial, food and restoration, the use of medicinal plant derivates (essential
oils, hydrolates, aqueous, alcoholic, and hydroalcoholic extracts) as biocidal substances has recently
grown up. The development of new materials and methods, which are eco-compatible, safe, and long-
lasting alternatives to those currently in use for surface protection and corrosion and biodeterioration
inhibition, represents a necessary response for the safety request not only of the protected asset but
also of the operator and the environment.
    In the last ten years, the data obtained from the available studies on the use of essential oils,
hydrolates, and plant extracts as biocides in the cultural heritage treatment are very encouraging.
The advantage of these natural products concerns the operators’ health safeguarding, in the reduction
of the environmental impact (air, water, soil), and in waste reduction. This review aims to provide
an overview of the biological and chemical exposition risk during the activities of prevention and
treatment of the fungal biodeterioration of artistic works and suggests the natural substances as a
possible alternative to chemical synthetic biocides to protect the restorer’s safety.

Biodeterioration

    The biological agents that produce biodeterioration (such as fungi, bacteria, mosses, lichens,
higher plants, and animals such as insects and rodents) are called biodeteriogens and can cause
irreparable damages to artifacts (Lognoli et al., 2002). Biodeterioration is the consequence of the
biocolonization process (formation of biofilm) which depends on the material’s “bioreceptivity”. This
last term was used for the first time by Guillitte (1995) to highlight the ability of a given material to be
colonized by living organisms. It depends on various parameters such as environmental conditions,
material composition and conservation state, and possible surface treatments. Bioreceptivity must
be considered, before any sustainable conservation procedure is performed, because it highlights the
relationships between the surface, the specific environment, and the organisms that thrive there. In
fact, a microbial community immersed in an extracellular polymeric matrix (biofilm), which adheres
irreversibly to a surface, has a high resistance to environmental stresses and treatments (Lo Schiavo
et al., 2020). These organisms develop in specific matrices based on their metabolic characteristics,
because the chemical composition of the matrices influences the selection and growth of biodeteriogen
populations in different ways. For example, organic materials (paper, wood, fabrics, parchments, etc.)
provide nutritional components for the growth of specific bacterial and fungal microflora (Görs et al.,

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2007; Fazio et al., 2010), while inorganic materials (stones, marbles, metals) undergo the action of
organisms that derive their nutritional source from occasional elements such as powders, resins, glues
or previous biological colonization, such as cyanobacteria, algae, lichens and heterotrophic bacteria
that form subaerial biofilms (Gorbushina and Broughton, 2009). The main biodeterioration cause is
the combination of atmospheric pollutants and fungi present on the artifacts depending on the nature of
the support material. The fungal biodeterioration mechanisms are related to: i) their ability to grow at
low values of water activity, which allows them to colonize different materials and ii) their metabolism
products, and molecules excretion (pigments, organic and inorganic acids, chelators, enzymes, and
extracellular polymeric substances), that modify the chemical-physical material properties causing
enzymatic hydrolysis of organic materials, biocorrosion, biomineralization and penetration into the
manufactured goods (Gómez-Alarcón et al., 1994; Kumar and Kumar, 1999; Sterflinger, 2000; Tiano,
2002; Görs et al., 2007; Sasso et al., 2013). In fact, fungi are able to colonize, degrade and alter a
great variety of materials used to create monuments and artifacts preserved in archives, museums, and
historic buildings (Sterflinger, 2010; Fierascu et al., 2012):
   - stone artworks (Kumar and Kumar, 1999);
   - paper (books, manuscripts, parchments) (Keopannha, 2008);
   - textile materials (Aranyanak, 1995);
   - leather, wood, bone, ivory, horn, and plasters (Florian, 2002).
   Several filamentous fungi, cellulase producers, can colonize wood artifacts (Fazio et al., 2010).
On atmosphere-exposed stone substrates, fungi, jointly with cyanobacteria and algae (phototrophic
partners), and heterotrophic bacteria, form specific microbial communities called “subaerial
biofilms” (Gorbushina and Broughton, 2009). Stone monuments surfaces can be altered by the
hyphae penetration through the porous matrix (Kumar and Kumar, 1999; Sterflinger, 2000) and by
the production of organic acids and pigments (Gómez-Alarcón et al., 1994). The stone artworks
colonization follows a very precise pattern that generally begins with first the colonizers autotrophic
organisms (algae, mosses, and lichens). These organisms are able to grow on surfaces damaged by
atmospheric agents using the stone mineral components, that progressively become more rough
and porous. Materials consequently lose cohesion weakening the structural resistance of the work
(Tiano, 2002). Such damage and alterations strongly depend on colonizing organisms, which are
favored by micro and macro environmental conditions (Caneva et al., 2008). The metabolism of
these first autotrophic colonizers generates a suitable microenvironment for the development of other
heterotrophic biodeteriogens such as fungi. These, in turn, completing their life cycle, enrich the
stone with organic matter and growth factors useful for the development of other microorganisms as
well as the plant organisms, from cryptogams to higher plants. The biodeterioration phenomena on
stone works include mechanical damage (breakage and loss of cohesion of the support), chemical
alteration (excretion of metabolites), and aesthetic damage (formation of patinas and crusts) (Caneva
et al., 2008; Salvadori and Municchia, 2016).
   Fungi are the primary colonizers of paper works (books, manuscripts, parchments) stored in
archives, museums, and historic buildings where poor ventilation and moist can create an environmental
microclimate suitable to the germination and growth of airborne spores and spores present in the dust
(Kaarakainen et al., 2009). The fungal spores may survive for a long time in a dormant phase. Their
germination occurs under favorable temperature and humidity conditions (63-80% of relative humidity
and temperature between 20-35 °C). However, these indoor fungal species may experience significant
variations related to seasonality and environmental conditions (Gupta et al., 2021). Fungi commonly
found on paper and books are slow growing species of Ascomycetes (Eurotium) and mitosporic
xerophilic fungi (Aspergillus, Paecilomyces, Chrysosporium, Penicillium, Cladosporium, etc.), that
thrive in materials with low water activity (aw 0.70–0.85). These fungi can cause allergic reactions

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in exposed workers (Polo et al., 2017). When humidity becomes higher to 65%, these fungi can be
superseded from other species (Chaetomium spp., Monoascus spp., Epicoccum spp., Trichoderma spp.
and Stachybotrys spp.) (Pinzari and Montanari, 2011; Montanari et al., 2012; Saifeldin et al., 2014). The
major fungal species causing damages in art works are mentioned in supplementary Table S1 (Schmidt
and Schaechter, 2012; Sterflinger and Piñar 2013; Saifeldin et al., 2014; Isola et al., 2022).

   Resolving interventions against fungi require the adoption of emergency and monitoring
procedures as well as appropriate intervention measures. Environmental control measures, such as
relative humidity monitoring, and cleaning, can avoid the development of biocontaminants and the
growth on the artifact. Although prevention is the best approach to conservation, in the event of an
accident (floods, torrential rains, etc.) a fungicide treatment is required. Biodeterioration is a problem
that must be managed with two objectives:
   - accurately understanding the causes that lead to the uncontrolled growth of macro and/or
microorganisms (diagnosis).
   - developing appropriate methodologies to slow or remove unwanted biological growth (therapy).
   The biodeteriogen control methods can be divided into direct and indirect. Indirect methods control
microbial growth by acting on environmental factors (water, light, temperature, humidity, nutrients,
pollutants, etc.). The direct methods directly target the biodeteriogenic agent and can be mechanical
(spatula or brush chisel removal), physical (280-240 nm UV radiations), and chemical (biocides).

Effects on Workers

The presence of biodeteriogens may expose the sector operators to biological agents, while the
restoration activities may expose them to physical and chemical agents, the latter represented by
chemical biocides.

Biological risk
Although biological risk in the workplace is often present, it is frequently underestimated, particularly
in work activities where biological agent exposure is an undesired but inevitable phenomenon. In
fact, with the exception of sectors where the presence of biological agents is evident (health care,
veterinary medicine, research, animal husbandry, waste disposal) several activities may appear to
be exempt from this occupational risk. It is important to highlight that a proper assessment of the
biological risk requires the analysis of various factors, which due to the difficulty of standardised
measurements and exposure limit values are not always ponderable. In fact, both the biological
agent characteristics (pathogenicity, infectivity, transmissibility, neutralization), and individual
susceptibility (immunosuppression, drug use, lifestyle, etc.) must be evaluated. Furthermore, the
different exposure scenarios, transmission routes, doses, and exposure duration are significant. As a
result, it is therefore evident that the operator exposure modalities are the parameters on which to base
workplace prevention and protection activities (Ciferri, 1999; Urzì, 2000; Palla et al., 2002; Suihko
et al., 2007; Pinar et al., 2009; De Leo et al., 2012; Pangallo et al., 2012).
   The biological risk exposure scenarios are various and diversified and include work activities
in outdoor environments, that could expose workers to the presence of potentially harmful animals
(rats, insects, reptiles), and indoor environments (underground excavations, archives, libraries).
In these last cases, the climatic conditions (temperature, relative humidity) may provide an ideal
habitat for the growth of species releasing spores and allergens, such as micro-fungi, bacteria, and
viruses. Restoration workers, in particular, may be susceptible to respiratory diseases or, more rarely,
dermatitis (Table 1).

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Table 1. – Pathologies, in restoration activities, related to fungi and bacteria exposure (Modified from: Johanning et al.,
2014).

 Organ / System                      Patologies                                         Agents
 Upper respiratory tract: nose,      Rhinitis, sinusitis, laryngitis                    Fungi, allergens, particulates,
 sinuses, throat                                                                        volatile organic compounds of
                                                                                        microbial origin
 Lower respiratory tract: lungs,   Bronchitis, asthma, bronchiolitis, allergic          Fungi, allergens, fine dust,
 bronchial system, alveoli         bronchopulmonary aspergillosis, extrinsic            fungal by-products
                                   allergic alveolitis (or hypersensitivity
                                   pneumonitis)
 Upper and lower respiratory tract Fungal rhinosinusitis, aspergillosis                 Fungi, allergens, fine particles
 Skin and mucous membranes         Urticaria, dermatitis, conjunctivitis                Fungi, allergens
 Central nervous, immune, and      Cognitive and psychiatric disorders, hepatitis,      Fungi, microbial products,
 endocrine systems, liver, kidneys nephritis, changes in the menstrual cycle, and       mycotoxins, organic powders
                                   thyroid function

   In particular, several fungi can trigger allergies and respiratory diseases already after short
exposures or, in the case of long or intense exposure, they may induce more serious pathologies
(allergic bronchopulmonary aspergillosis or hypersensitivity pneumonitis) (Samson, 1985). Such
pathologies, as shown in the Table 2, are mainly attributable to exposure to aerosols containing fungi,
their propagules, or their by-products.

Table 2. – Fungal components and products relevant for pathologies attributable to aerosols exposure (Modified from:
Nevalainen and Taubel, 2015).

 Etiological Agents                                                                    References
 Fungal origin fragments size less than the spores (< 1 µm)                            Gorny et al. 2002
                                                                                       Gorny 2004
                                                                                       Méheust et al. 2014
 β-D-Glucans (structural components linked to D-glucose polymers of the fungal wall) – Douwes et al. 2000
 induce a proinflammatory activity
 Fungal allergens (antigenic compounds) – stimulate the IgE-mediated immune response Williams et al. 2016
                                                                                       Crameri et al. 2009
 Volatile organic compounds of microbial origin, highly volatile chemicals (alcohols,  Korpi et al. 2009
 aldehydes, amines, ketones, terpenes, and aromatic hydrocarbons) produced by the      Schleibinger et al. 2008
 fungi growth as primary or secondary metabolites                                      Persoons et al. 2010
                                                                                       Inamdar et al. 2020
 Mycotoxins (secondary non-volatile metabolites), varieties of chemical compounds      Amuzie et al. 2008
 bioactive or toxic by ingestion or inhalation                                         Wong et al. 2016

   Hypersensitivity pneumonitis is characterized by the immune-complexes formation determined by
antigens of microbial origin (Table 3) (Kleyn et al., 1981; Cormier et al., 1998; Bertorelli et al., 2000;
Yoshikawa et al., 2006; Enríquez-Matas et al., 2009; Ficociello et al., 2019).




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Table 3. – Hypersensitivity pneumonitis and etiological agents (Modified from Mahmoudi, 2016).

 Correlation between pathology and specific antigens of organic nature exposure
 Antigen                                                      Source                       Pathology
 Thermophilic actinomycetes (Saccharopolyspora                Plant compounds (moldy       Farmer’s lung
 rectivirgula / Micropolyspora faeni, Thermoactinomyces hay, grain, silage), foliage
 vulgaris, T. viridis, T. candidus, T. sacchari), Fusarium    and dry herbs, fertilizer,
 spp., Penicillium brevicompactum, Saccharomonospora          moldy forage
 viridis, Absidia cerymbifera, Wallemia sebi
 Thermophilic actinomycetes (Saccharopolyspora                Compost for mushrooms,       Mushroom worker’s lung
 rectivirgula /Micropolyspora faeni, Thermoactinomyces        indoor mushrooms
 vulgaris, T. viridis, T. candidus, T. sacchari), Monocillium cultivation, peat
 spp., Basidiospores of: Pleurotus ostreatus, Hypsizygus
 marmoreus, Lycoperdon perlatum
 Penicillium expansum, P. cyclopium, P. chrysogenum,          Moldy wood and wood          Woodworker’s lung
 Acremonium spp., Alternaria spp.                             dust
 Aspergillus spp., A. clavatus                                Moldy barley                 Malt worker’s lung
 Aspergillus spp., Penicillium spp.                           Greenhouse soil              Greenhouse worker’s lung
 Penicillium casei, P. roqueforti, P. cyclopium, P.           Cheese molds, salami         Dairy workers’ lung, Salami
 chrysogenum, P. camemberti                                   molds                        seasoners’ lung

   In Italy, the Ministerial Decree of June 10, 2014 recognizes organic dust syndrome as an
occupational disease, an acute non-allergic pulmonary inflammatory reaction attributable to exposure
to fungal spores. Its symptoms arise without any previous sensitization and it is caused by inhalation
of toxins produced by fungi or other contaminants of organic dust (Langley, 2011; Piecková, 2012;
Rando et al., 2012).
   It is also known that some fungal species producing mycotoxins frequently colonize indoor
environments. Throughout the past few years, attention has been paid to the exposure to mycotoxins
in indoor work environments. Mycotoxins are secondary fungal metabolites that contain a large set
of organic compounds (alkaloids, cyclopeptides, coumarins, phenols, and terpenoid). Mycotoxins are
therefore a risk factor that is currently unknown and most likely underestimated. Indeed, mycotoxins
are not very volatile and human exposure is predominantly linked to the contaminated food ingestion.
However, the possibility that a potential exposure route could be inhalation, carried by spores or
contaminated substrates, cannot be excluded (Sorenson et al., 1981; Dvorackova and Pichova, 1986;
Wangia et al., 2019). Their presence depends on environmental factors and microclimatic conditions.
Cases of pulmonary mycotoxicosis have been reported in agricultural and textile workers.
   Lougheed et al. (1995) were perhaps the first to associate cases of lung disease with the presence
of aflatoxin B1 due to the exposure to a work environment contaminated by Fusarium species (Saad-
Hussein et al., 2013; Ferri et al., 2017; Masciarelli et al., 2020). Although Penicillium and Aspergillus
species are the most prevalent fungal contaminants in indoor environments, there are also less common
fungal species such as Stachybotrys and Chaetomium that are being investigated for their effects on
health, due to chronic long-term exposure (Table 4) (Jarvis and Miller, 2005; Fromme et al., 2016).




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Table 4. – Mycotoxins and fungi producing mycotoxins in indoor environments are significant to occupational purposes
(Modified from Fromme et al., 2016).

 Mycotoxins                            Some fungal species producing mycotoxins              Toxicity
 alternariol, alternariol monomethyl   Alternaria spp., A. alternata                         Genotoxic,
 ether, altenuene (and other less                                                            teratogenic,
 frequent)                                                                                   carcinogenic

 Atranoni A-K                          Stachybotrys chlorohalonata, S. chartarum             Pro-inflammatory
                                       (chemotype A)                                         action
 Beauvericin                           Beauveria bassiana, Paecilomyces fumosoroseus,        Cytotoxic and
                                       Fusarium spp.                                         immunotoxic
 Chetoglobosine, chaetomina,           Chaetomium spp. C. globosum                           Cytotoxic
 chaetoviridine
 Enniatine                             Fusarium spp.                                         Cytotoxic and
                                                                                             immunotoxic
 Fumitremorgine                        Aspergillus fumigatus                                 Tremors
 Gliotoxin                             Aspergillus spp., A. fumigatus                        Cytotoxic and
                                                                                             immunosoppressive
 Mycophenolic Acid                     Penicillium spp., P. brevicompactum, P. roquefortii   immunosoppressive
 Penitrem A                            Penicillium spp.                                      Tremors
 Roquefortine C                        Penicillium roquefortii, P. chrysogenum               Neurotoxic
 Roridine (E e L-2)                    Stachybotrys chartarum (chemotype S)                  Cytotoxic and
                                                                                             immunosoppressive
 Satratozin (G, H, F)                  Stachybotrys chartarum (chemotype S)                  Cytotoxic and
                                                                                             immunosoppressive
 Sterigmatocystin                      Aspergillus versicolor                                Carcinogenic
 Trichotecenes                         Stachybotrys chlorohalonata, S. chartarum             Cytotoxic
                                       (chemotype A), Memnoniella echinata
 Verrucarin                            Stachybotrys, Fusarium, and Myrothecium               Cytotoxic and
                                                                                             immunosoppressive
 Verrucologen                          Aspergillus fumigatus, Penicillium spp.               Tremorgenic

    Experimental studies on the mycotoxins inhalation have shown the induction of a rather wide
spectrum of adverse reactions: mucous, membrane irritation, endocrine and immune system alterations,
renal failure, fever, asthenia, nausea. The presence of mycotoxins in indoor environments has also
been linked to Sick Building Syndrome, particularly in relation to some Stachybotrys chartarum
strains able to produce different mycotoxins (roridina E and L-2, satratozina F, G, and H, isosatratoxin
F, G, and H, verrucarine B and J, tricoverrole A and B, tricoverrins A and B, atranone B) (Hardin et
al., 2003). These fungal species, for grow, require substrates with a high cellulose content (fabrics,
paper, glue, bookbinding), a low nitrogen content, and a relative humidity higher than 55% (Gorny
et al., 2002; Brasel et al., 2005).
    The presence of fungi producing mycotoxins should be underestimated even in underground
excavation environments, museum deposits, archives, and libraries where dust, poor air exchange,
and humidity can favour the presence of pathogenic fungi. Other frequently encountered pathologies
are allergic and non-allergic dermatitis, in rare cases manifestations of scabies due to the manipulation
of fibrous materials (fabrics, paper, etc.), and conjunctivitis caused by microorganisms present in the
dust or by rubbing eyes with dirty hands.

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Chemical risk
To stop the degradation caused by microorganisms and organisms or to delay their appearance,
restoration interventions imply the use of biocides, composed of active ingredients, co-formulates,
and solvents (Marconi et al., 2019).
    Biocide (Table 6) or “biocidal product means any substance or mixture, in the form in which it
is supplied to the user, consisting of, containing or generating one or more active substances, with
the intention of destroying, deterring, rendering harmless, preventing the action of, or otherwise
exerting a controlling effect on, any harmful organism by any means other than mere physical or
mechanical action” and “any substance or mixture, generated from substances or mixtures which
do not themselves fall under the first indent, to be used with the intention of destroying, deterring,
rendering harmless, preventing the action of, or otherwise exerting a controlling effect on any harmful
organism by any means other than mere physical or mechanical action” (Regulation (EU) 528/2012).
    The biocide choice has to be made evaluating:
    - pathogenic organism/s;
    - the artifact’s constituent materials;
    - the artifact’s preservation state (see Table 5).

Table 5 – Most used biocides in Italy (supplemented and modified from Bartolini et al., 2007; Coutinho et al., 2016;
Favero-Longo et al., 2017; 2018; Pinna, 2017; Kakakhel et al., 2019; Lo Schiavo et al., 2020; Franco-Castillo et al., 2021).

 Commercial product      Composition                                                               Action spectrum
 Preventol RI 80 (CTS)   N-Alkyl-N-benzyl-N,N-dimethylammonium chloride                            Fungi, bacteria, and
                         (benzalkonium chloride) approx. 80% + isopropyl alcohol (2%)              algae
                         in water
 Biotin T (CTS), Rocima™ N-Decyl-N,N-dimethyldecan-1-aminium chloride (Didecyl-                    Lichens, fungi,
 103                     dimethyl ammonium chloride) (40–60%) + 2-octyl-4-                         bacteria, and algae
                         isothiazolin-3-one (OIT) (7–10%) + isopropyl alcohol (15–
                         20%) + formic acid(2.0–2.5%)
 Lichenicida 464         4,5-dichloro-2-octyl-4-isothiazolin-3-one (DCOIT) (25– < 40%)             Lichens
                         + 3-iodo-2-propynyl N-butylcarbamate (IPBC) (12.5– < 15.0%)
                         + 2-octyl-4-isothiazolin-3-one (OIT) (0.06– < 0.10%) + benzyl
                         alcohol (40– < 60%)
 Biotin R (CTS)          3-iodo-2-propynyl N-butyl carbammate (IPBC) (10–25%);                     Fungi, bacteria, and
                         2-octyl-4-isothiazolin-3-one (OIT) (3–5%); in diethylene glycol           algae
                         butyl ether
 Sinoctan PS             4,5-dichloro-2-octyl-4-isothiazolin-3-one (DCOIT) + 3-iodo-2-             Fungi, bacteria,
                         propynyl N-butylcarbamate (IPBC)                                          mosses, lichens, and
                                                                                                   algae
 Algophase                     2,3,5,6-tetrachloro-4-(methylsulfonyl)pyridine (TCMSP) (30%)        Lichen, algae
                               + N-methyl-2-pyrrolidone

   Generally, the action mechanism of biocides consists in blocking cell wall synthesis and causing
damage to DNA and RNA, therefore they are often also toxic to humans and the ecosystem (Guardiola
et al., 2012; Kakakhel et al., 2019; Galvão de Campos et al., 2022). Potentially, restorers may be
exposed to these compounds but there is a lack of data on biocides exposure and the possible health
impacts on this category of workers (Varnai et al., 2011). Chemicals’ potential adverse effects on
human health are linked, in addition to their intrinsic toxicity, to factors such as their chemical/physical
properties, their concentration of use, the exposure routes and duration, the environmental conditions
(humidity, temperature, absence adequate air changes), the interaction with other substances, and the

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receiving organism’s capacity to absorb, metabolize and excrete, according to individual susceptibility
(age, weight, sex, genetic factors, any pathologies present, etc.). In particular, the exposure levels to
which a restoration worker may be subjected depend on the type of artifact to be restored, its state
of deterioration, the techniques used (brush, pack, injection, spray, or fumigation treatments), the
quantities of chemical products used, and the possibility of transporting the artifact to an adequately
equipped for safety purposes restoration laboratory.
    The biocides commonly used by restorers are based on quaternary ammonium salts, carbamates,
and isothiazolinones. Quaternary ammonium salts are inexpensive cationic biocides with relatively
low toxicity, but with a short-lasting effect, such as alkyl-dimethyl-benzyl ammonium chloride
(benzalkonium chloride) (Table 6), a powerful disinfectant-germicide effective on bacteria Gram+,
Gram-, fungi, and microflora in general. Benzalkonium chloride is therefore used for the cleaning and
disinfection of surfaces in glass, ceramics, stone materials, metals, synthetic and natural rubber, textile
fibers, and paper, and for the room disinfection. Being soluble in water (ethyl, methyl, and isopropyl
alcohol too), it is used above all in an aqueous solution or in formulation with other products (animal
glues or mush for re-lining of paintings). However, benzalkonium chloride is corrosive to the eyes,
skin, and the respiratory tract. In short-term exposure, aspiration into the lungs can lead to chemical
pneumonitis. In a fire event, furthermore, thermal decomposition produces toxic and corrosive fumes
of ammonia, chlorine, and nitrogen oxides.
    Isothiazolinones (isothiazol-3-ones), such as 2-octyl-4-isothiazolin-3-one (OIT), and 4,5-dichloro-
2-octyl-4-isothiazolin-3-one (DCOIT), are widely known as humans strong skin sensitizers due to
their irreversible reaction with proteins’ cysteine residues (Alvarez-Sánchez et al., 2003; 2004). Due
to their strong bactericide, fungicide, and algaecide properties, they are present in a wide range of
commercial products for everyday life, therefore they are used in many industrial sectors (textiles,
paints, glues, detergents, and leather tanning) where several cases of allergic contact dermatitis have
been detected on workers (Schwensen et al., 2020; Silva et al., 2020). Several studies on cell lines
investigated the potential cytotoxic effects of these substances. Kim et al. (2021) performed in vitro
studies on a blood-brain barrier (BBB) model treated with OIT, suggesting that constant exposure
to OIT may represent a risk of vascular or neurological diseases. In a previous study by Arning et
al. (2008) the effects of OIT and DCOIT on the human hepatoblastoma cell line Hep G2 and on the
glutathione (GSH) / oxidized glutathione (GSSG) ratio within the cell determined by the enzyme
glutathione reductase were tested. The obtained results showed that the DCOIT effects are greater than
those of OIT. DCOIT significantly reduces the GSH content in HepG2 cells in a dose/time dependent
manner and simultaneously increases the GSSG level. This causes a significant variation in the GSH/
GSSG ratio which can be the reason for necrosis and subsequent cell lysis. Often, isothiazolinones
are found in mixtures with carbamates (organic compounds characterized by the functional group –
NHCOO–) such as 3-iodo-2-propynyl N-butyl carbamate (IPBC) (Table 6) (Aronson, 2016). Cases
of allergic contact dermatitis have been attributed to this compound (Badreshia and Marks, 2002;
Jensen et al., 2003; Schöllnast et al., 2003; Davis and Johnston, 2007; Henriks-Eckerman et al., 2008).
Several cases of contact dermatitis have also been attributed to 2,3,5,6-tetrachloro-4- (methylsulfonyl)
pyridine (TCMSP), an active ingredient present in the Algophase (Table 6) used as an antimicrobial
(Sesseville et al., 1996; Le Coz et al., 1998; Huh et al., 2001; Gushi et al., 2003; Inoue et al., 2008).
The UK Advisory Committee on Pesticides has listed TCMSP as a skin irritant and a severe eye
irritant (Advisory Committee on Pesticides, 2004).




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Natural substances use in the restoration

In recent decades, there has been a growing demand for natural and eco-friendly biocides with long-
term efficacy and no adverse effects on cultural heritage or operator health. Natural or biologically
derived products that can act as biocides can have different origins:
    - natural molecules with biocidal activity (zoosteric acid, capsaicin, extracellular enzymes,
hydrolase, usnic acid, parietin, or bacterial extracts) (Bruno et al., 2019; Cappitelli et al., 2020).
    - microorganisms (biocleaning: predation processes operated by bacteria, removal of biofilms
by fungi, bacteriophages and viruses with antialgal activity; biomineralization: carbonatogenesis or
autotrophic or heterotrophic calcite production by bacteria) (Le Métayer-Levrel et al., 1999; Klaassen
et al., 2008; May et al., 2011; Charola et al., 2011; Zammit et al., 2011; Hu et al., 2013; Krakova et
al., 2015; Páramo-Aguilera et al., 2015; Silva et al., 2017; Jurado et al., 2020).
    - essential oils and plant extracts alone, incorporated in sol/gel matrices or applied by a polyphasic
approach to enhance their effectiveness (Veneranda et al., 2018; Jurado et al., 2020; Palla et al., 2020;
Sparacello et al., 2021).

   Essential oils, known since ancient times for their antimicrobial-repellent properties (Petrovska,
2012), may be used to counteract biological colonization (Bakkali et al., 2008; Nerio Quintana et al.,
2009) by regulating intermediate metabolism, activating or blocking enzymatic reactions, having
direct effects on enzymatic synthesis, or by altering the membrane structure (Bakkali et al., 2008;
Reichling et al., 2009).
   Many researchers are currently interested in using low environmental impact biocides such as plant
extracts as part of an eco-friendly approach to restoration. As an alternative to the use of synthetic
products, the use of natural and non-destructive treatments such as essential oils, hydrolates, and
plant extracts, seems to be a valid alternative for the health protection of environment and restoration
operators (Satish et al., 2007; Axinte et al., 2011; Afifi, 2012; Fierascu et al., 2012; Fierascu et al.,
2013). Tables 6 and 7 show the most significant studies.

Conclusions

In cultural heritage conservation, the risk prevention management of operators is particularly
articulated. In fact, despite knowing the hazard sources and risks connected with the conservation
operations, defining risk profiles and quantifying them for potentially correlated pathologies is not
entirely clear. This context necessitates research into organizational and procedural strategies, as
well as the application of appropriate protective equipment, to prevent and decrease risks, enhance
working conditions, and ensures the safety of people involved in the restoration and preservation of
cultural heritage.
   The use of natural products in the control and restoration of artifacts attacked by fungi fits perfectly
into a world that is globally shifting its attention to green approaches in various productive sectors in
order to safeguard human health and the environment. Recent studies have shown that essential oils,
hydrolates, and plant extracts are effective against fungi that deteriorate building materials. Therefore,
the application of essential oils or their active components could be a good option for contaminated
walls or other surfaces disinfection. However, there are scarce studies on their use in the conservation
of cultural heritage (Gatenby and Townley, 2003; Rakotonirainy and Lavédrine, 2005; Chung et al.,
2018; Fidanza and Caneva, 2019).




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Table 6 – Efficacy on fungal strains of essential oils (EOs) and hydrolates.

 Source of essential oils (EOs) and    Fungal strains                          Results                                                Authors
 hydrolates
 Pimpinella anisum, Syzygium           Aspergillus niger, Aspergillus          EOs of P. anisum and S. aromaticum, extremely          Borrego et al. 2012 - air samples and documents
 aromaticum, Cuminum cyminum,          clavatus, Penicillium sp.,              effective antifungals, less L. nobilis and C. sinensis National Archives of Cuba; Historical Archives of
 Allium sativum, Laurus nobilis,       Fusarium sp.                                                                                   the Museum of La Plata, Argentina
 Citrus sinensis, Origanum vulgare
 Abies sibirica, Carum carvi,          Penicillium sp., Aspergillus sp.,       S. aromaticum, higher antifungal activity, followed Levinskait et al. 2013 - stone material of the walls
 Mentha piperita, Eucalyptus           Cladosporium sp.                        by A. sibirica and C. carvi; T. pulegioides         of the historic city of Vilnius in Lithuania
 globulus, Thymus pulegioides,                                                 inhibition especially on Penicillium sp.; S.
 Syzygium aromaticum, Citrus                                                   aromaticum better than chemical treatments
 bergamia
 Melaleuca alternifolia, Lavandula     Cladosporium cladosporioides,           M. alternifolia, L. angustifolia, R. officinalis and   Mansour 2013 - stone sarcophagus Behbeet el-
 angustifolia, Rosmarinus              Paecilomyces variotii, Curvularia       O. vulgare completely inhibited the tested fungi       Hager, El-Gharbieh, Egypt
 officinalis, Origanum vulgare         lunata
 Origanum vulgare                      Aspergillus spp., Penicillium spp.      strong antifungal potential, equal or greater than     Stupar et al. 2014a - frescoes of the Holy Virgin
                                                                               benzalkonium chloride                                  Church in Serbia
 Ocimum basilicum                      Aspergillus sp., Penicillium sp.,       hydroalcoholic extracts better than EOs                Fierascu et al. 2014 - paper artifacts in Romania
                                       Mucor spp.
 Thymus capitatus                      Candida albicans, Fusarium              The best the harvests of June and July against F.      Casiglia et al. 2015 - Sicilian historical-artistic
                                       oxysporum, Aspergillus niger            oxysporum e A. niger                                   craftsmanship
 Origanum vulgare                      Fusarium sp., Scopulariopsis sp.        The under-study EOs vapors temporarily reduced         Lavin et al. 2016 - Historical Cartographic
 Thymus vulgaris                                                               or halted the growth of Scopulariopsis sp. e           Research of Geodesy, Buenos Aires; Museum of
                                                                               Fusarium sp.                                           Historical Archive, La Plata, Argentina
 Origanum vulgare, Thymus              Black fungi                             EOs better than benzalkonium chloride                  Devreux et al. 2016 - bench with a female bust,
 vulgaris (EOs in an organic                                                                                                          located in the Zitella area of the Vatican Gardens
 solvent, individually or
 synergically)
 Origanum vulgare                      Aspergillus spp.                        EOs of O. vulgare showed greater antifungal            Savković et al. 2016 - Sculpture, brick and stone
                                                                               activity than the commercial biocide Sanosil S003      walls, silk icon, archivial papers, Serbia



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Table 6 – Efficacy on fungal strains of essential oils (EOs) and hydrolates (continue)

 Source of essential oils (EOs)       Fungal strains                      Results                                                Authors
 and hydrolates
 Melaleuca alternifolia               Penicillium chrysogenum,            EOs M. alternifolia activity against P. chrysogenum,   Rotolo et al. 2016 - colonized artworks
                                      Aspergillus spp.                    no vs Aspergillus spp.
 Origanum majorana,                   Aspergillus niger, Alternaria       C. camphora and S. aromaticum EOs efficient on         Elsayed and Shabana 2018 - oil paintings and other
 Cinnamomum camphora,                 alternata                           both fungi.                                            cultural heritage objects
 Syzygium aromaticum, Ocimum
 basilicum
 Cinnamomum zeylanicum                Aspergillus niger, Penicillium      Vapors of EOs treatment without altering the           Matusiak et al. 2018 - Four fabric objects (Museum
                                      funiculosum, Trichoderma viride     characteristics of the tissues                         of Archeology and Ethnography, Lodz, Poland)
 Origanum vulgare, Thymus             Aspergillus flavus                  EOs better than synthetic biocides (benzalkonium       Palla et al. 2020 - wooden works bio- deterioration
 vulgaris                                                                 chloride and Nipagin-M)
 Azadirachta indica, EOs and          Aspergillus flavus                  Neem seed EOs result more effective than Neem          Gupta et al. 2021 - old manuscript of the National
 Neem seeds ethereal extracts                                             seed extracts                                          Research Laboratory India
 (ethyl ether)
 Emulsion of 0.3% Cinnamomum          Aspergillus niger,                  Sprayed on the painting’s back and left to act for     Minotti et al. 2022 - ancient oil paintings restoration
 zeylanicum EOs and 99.7% Citrus      Aureobasidium pullulans,            24 hours without altering the painting’s chemical-     (“The Silence” by Jacopo Zucchi kept at the Uffizi
 aurantium var. amara hydrolate       Chaetomium globosum,                physical characteristics                               Museum in Florence)
                                      Cladosporium cladosporioides,
                                      Alternaria alternata, Penicillium
                                      citrinum
 GELYD (Monarda fistulosa e           Aspergillus sydowii, Penicillium    with M. fistulosa and C. aurantium var amara         Di Vito et al. 2017; 2018
 Citrus aurantium var amara           chrysogenum, Cladosporium           hydrolates, fungicidal action only with C. aurantium
 hydrolates added with Gellan         cladosporioides                     for paper cleaning and bioattack preventing.
 hydrogel
 Citrus limon, Mentha spicata,        Saccharomyces cerevisiae,           C. limon and M. spicata; P. vulgare, O. majorana. R. Sakr et al. 2012 - paintings in the royal tombs of
 Phoeniculum vulgare, Origanum        Candida albicans, C. lipolytica,    officinalis no effect                                Tanis in Egypt 840 BC
 majorana, Rosmarinus officinalis     Lodderomyces elongisporus




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Table 7. - Efficacy on fungal strains of plant extracts (EOs essential oils, HE Hydroalcoholic Exstract, CE Choloform Exstract).

 Plant extracts                     Fungal strains                 Results                                              References
 Calamintha nepeta                  Penicillium chrysogenum        C. nepeta shows very low activity against fungal     Rotolo et al. 2016 - colonized artworks
 Allium sativum                     Aspergillus sp.                strains; A. sativum exhibits high activity against
                                                                   both strains at all concentrations tested

 Anethum graveolens                 Fusarium oxysporum             C. citrates shows more significant inhibitory        Afifi 2012 - stucco ornaments in the Mihrab of Mostafa
 Cymbopogon citrates                Aspergillus niger              activity on all fungal species tested; A. graveolens Pasha Ribate, Azdomor Al Salehy, Egypt
 Juniperus oxycedrus                Alternaria alternata           only retarded the fungi growth; J. oxycedrus was
                                                                   found to be the least effective; A. alternata, more
                                                                   resistant strain; F. oxysporum most sensitive strain

 Synadenium grantii                 Cladosporium                   S. grantii and C. variegatum extracts reduced all Mansour 2013 - stone sarcophagus Behbeet el-Hager, El-
 Codiaeum variagatum                cladosporioides                organisms tested growth; S. grantii CE is the most Gharbieh, Egypt
                                    Paecilomyces variotii          effective
                                    Curvularia lunata


 Ocimum basilicum                   Aspergillus sp.                HE showed better antifungal activity, followed       Fierascu 2014 - paper artifacts, Romania
 hydroalcoholic and aqueous         Penicillium sp.                by EOs, and finally by aqueous extracts. The HE
 extract                            Mucor sp.                      has longer-term effects than EOs; HE more safe,
                                                                   efficient and less expensive as fungicidal than
                                                                   EOs




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   The use of essential oils as new biocidal agents in cultural heritage conservation has the advantage
of a low environmental permanence, but some of them, at high doses, are toxic or even neurotoxic
for humans, therefore their use cannot be separated from the use of adequate protective equipment
(gloves, mask, goggles, and overalls). Essential oils are also very expensive, unlike hydrolates, which
are by-products of their production. Vegetable extracts, on the other hand, not only have a high biocidal
activity, but are also inexpensive and simple to prepare from cultivated and wild officinal plants
found in the territory. Because of their strong antibacterial activity, minimal mammalian toxicity, and
biodegradability, hydrolates and plant extracts could be effective alternatives to synthetic biocides
(Saxena and Mathela, 1996). However, further studies are needed to develop adequate use methods
of these substances in the conservation of cultural heritage and, particularly, in the fungi treatment
(Stupar et al., 2014b).
   It would also be desirable to develop good preventive conservation practices on all cultural heritage
artifacts including good cleaning methods, custody, dusting, periodic control, and prevention of any
possibility of physical, chemical, and biological damage. Preventive conservation plays a crucial role
and can take on great importance in every country with a rich cultural heritage. A diagnosis made in
time and adequate preventive measures can solve and/or eliminate many problems.

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