Concerns regarding indoor air quality, particularly the presence of fungi and moulds, are increasing. The potential for essential oils to reduce, control or remove fungi, is gaining interest as they are seen as a “natural” alternative to synthetic chemical fungicides. This review examines published research on essential oils as a method of fungal control in indoor environments. It was difficult to compare the relative performances of essential oils due to differences in research methods and reporting languages. In addition, there are limited studies that scale up laboratory results and assess the efficacy of essential oils within building environments. However, generally, there appears to be some evidence to support the essential oils clove oil, tea tree oil, oregano, thyme and lemon as potential antifungal agents. Essential oils from heartwood, marjoram, cinnamon, lemon basil, caraway, bay tree, fir, peppermint, pine, cedar leaf and manuka were identified in at least one study as having antifungal potential. Future studies should focus on comparing the effectiveness of these essential oils against a large number of fungal isolates from indoor environments. Studies will then need to focus on translating these results into realistic application methods, in actual buildings, and assess the potential for long-term antifungal persistence.
Indoor air quality is a public health issue of increasing concern (1), (2), (3). One of the leading indoor air quality complaints is the presence of fungi and moulds, which have been associated with increased risk of adverse health effects (4), (5). The most common adverse health effects associated with fungi in indoor environments, as recently reviewed by Nevalainen et al. (6), are various respiratory conditions. Other potential health effects include allergic responses, infection or toxigenic effects, for which the pathophysiology is less evident (2). Of these, infection and toxicity have serious consequences but are rare in occurrence, whereas allergic responses are commonly observed (7). These allergic responses include rhinitis, eye irritation, cough and aggravation of asthma, which is of emerging significance given that the incidence of asthma in children from developed countries is increasing (8), (9), (10). Burr et al. (11) conducted a randomised control trial to explore the effect of eradicating visible mould from the homes of asthma patients. It was found that the symptoms of asthma and rhinitis improved and medication usage decreased in the patients who had indoor mould removed, fungicide applied and a fan installed in the loft of their homes.
Fungi and moulds have also been demonstrated to contribute to sick building syndrome and other building related illnesses (7), (12). Sick building syndrome is recognised as a group of symptoms (e.g. eyes, nose and throat irritation; dry skin, headache and lethargy) that are related to spending time in a particular building. This is more commonly identified in offices; however, there have been reports of sick building syndrome in schools, hospitals, care homes and domestic houses (13). Research has demonstrated that one of the key risk factors of sick building syndrome is dampness, which promotes mould growth (14).
To reduce the potential risk of exposure, indoor areas with visible fungal growth must be immediately remediated (15). Early intervention for fungal contamination is essential; otherwise, professional remediation will be required (3). Remediation typically involves the removal of building material with visible mould contamination, in conjunction with treatment of surfaces with an antifungal product. Remediation should also include steps to prevent moisture build-up, which enables future fungal growth (16). An antifungal agent (otherwise known as a fungicide) is a compound used to kill or inhibit the growth of fungi and/or fungal spores (sporicide) (17). Antifungal agents recommended for indoor environments should be non-toxic to humans, odourless and hypoallergenic (18). It is ideal that the antifungal agent also provides long-term protection from fungal regrowth, especially in humid or moist environments that would promote fungal growth; however, in reality, this long-term persistent protection is difficult to achieve especially for non-toxic fungicides (19), (20).
Globally, there is increasing concern regarding synthetic chemical usage and residue and the potential human health effects of exposure (21). Consequently, there is a push from consumers for ‘natural’ alternatives to chemical antifungal products for use in residential and commercial indoor environments (2), (15), (22). As such, research on essential oils and their potential antimicrobial capabilities has received increasing attention (23). Essential oils are complex mixtures of volatile compounds biosynthesised by plants, the main groups of which include terpenes and terpenoids and aromatic and aliphatic constituents, and are characterised by low molecular weight (24). Essential oils have been widely used in medicine and the food industry for their antimicrobial properties; however, there are limited studies investigating their use for the control of indoor air quality. The increased interest in natural substances is driving the research community to find new applications of these substances. The aim of this review was to examine studies that have investigated the antifungal potential of essential oils specifically as a method for improving indoor air quality for building occupants.
A search was conducted through the Scopus (25), ProQuest (1), Science Direct (6) and Web of Science (26) databases. The search terms included (mould OR mold OR fungi OR fungal OR fungus) AND (“indoor air” OR indoor OR building OR buildings) AND (“essential oil” OR “essential oils” OR “plant-derived compound” OR “plant extract”) AND (antifungal OR fungicidal OR fungicide OR sporicidal OR sporicide OR anti-microbial OR biocide OR biocidal), and the search was limited to the title, abstract and keywords. Figure 1 presents the systematic approach to article inclusion or exclusion. Articles were screened by reading titles and abstracts and initially excluded if they did not describe original research or did not examine the fungicidal activity of essential oils. Articles were then read in full and excluded if they described a fungal control not relating to indoor air or buildings (e.g. articles describing the control of clinical isolates, animal, crop or food spoilage, etc. were excluded). A total of 19 studies that described the antifungal potential of essential oils or their extracts for the purpose of influencing indoor air quality were included and are summarised in Table 1.
|Extracts from heartwood (Pinus rigida), eucalyptus leaves (Eucalyptus camaldulensis) and creper ginger rhizomes (Costus speciosus)||Alternaria alternata, Fusarium subglutinans, Chaetomium globosum, Aspergillus niger and Trichoderma viride||Wood specimens treated at the level of 2% concentration of heartwood extract observed good inhibition to the mould growth||(27)|
|Extracts from marjoram (Origanum majorana), thyme (Thymus vulgaris) and ginkgo leaves (Ginkgo biloba)||C. globosum (ATCC 6205), A. niger (ATCC 9642), Aureobasidium pullulans (ATCC 15233), Gliocladium virens (ATCC 9645) and Penicillium pinophilum (ATCC 11797)||Marjoram extracts demonstrated excellent antifungal performance in the laboratory experiments and when applied to the antifungal mortars||(28)|
|Extracts from myrrh (Commiphora myhrra)||Acremonium strictum, Aspergillus flavus, Aspergillus sydowii, C. globosum, Cladosporium cladosporioides, Cladosporium sphaerospermium, Cladosporium verrucocladosprioides, Cochliobolus spicifer, Drechslera biseptata, Embellisia chlamydospora, Eurotium amstlodami, Fusarium semitectium, Myceliophthora lutea, Penicillium chrysogenum, Penicillium fellutanum, Penicillium reticulosum, Phoma tropica, Torula caligans, Trichoderma psudokoningii and Ulocladium consortiale||The antifungal efficacy of myrrh was highly dependent on the sensitivity of the fungal species. The highest growth inhibition (74.6%) was against A. strictum and the lowest growth inhibition (12.7%) was against U. consortiale||(25)|
|Cavicide® and Virkon®, 70% ethanol, vinegar (4.0%–4.2% acetic acid) and tea tree oil (Melaleuca alternifolia)||Aspergillus fumigatus and P. chrysogenum||Tea tree oil demonstrated the greatest inhibitory effect on the growth of both fungi, followed by Cavicide®and Virkon®. Vinegar only inhibited P. chrysogenum and 70% ethanol had no inhibitory effect||(15)|
|Clove oil (Syzygium aromaticum)||Three white-rot fungi (Trametes hirsuta, Schizphylhls commne, and Pycnoporus sanguineus) (common causes of wood rot)||50 μg/g clove essential oil had 100% mortality to Reticulitermes chinensis after testing for 5 days||(29)|
|Cinnamon oil (Cinnamomum verum) and clove oil (S. aromaticum)||Aspergillus sp. (WU1003), Trichothecium sp. (WU1004), Trametes sp. (WU1005) and Gloeophylum sp. (WU1006)||3% concentration of cinnamon and clove oil gave complete inhibition against Aspergillus sp. and Trichothecium sp. on rubberwood particleboard for 9 weeks. Particleboards treated with clove or cinnamon oil were found to have reduced mass loss from Trametes sp. and Gloeophylum sp. compared to the controls. The percentage loss of mass decreased with increasing levels of clove and cinnamon oils||(30)|
|Cinnamon oil (C. verum) and clove oil (S. aromaticum)||Aspergillus sp. WU1003 and Trichothecium sp. WU1004||Dip treatment in cinnamon oil and clove oil at a concentration of 0.63% was capable of providing complete protection for at least 8 and 5 weeks, respectively. Contents of cinnamaldehyde and eugenol in the particleboards, the main antifungal agents in cinnamon oil and clove oil, respectively, largely declined within the first 4 weeks of incubation, which could explain the time limit of the fungicidal activity||(31)|
|Oregano (Origanum vulgare) essential oil||A. fumigatus, Aspergillus nidulans, Aspergillus versicolor and one Penicillium species||Oregano demonstrated strong antifungal activity against all fungal isolates tested; however, it was not as effective as biocide and benzalkonium chloride||(32)|
|Essential oils from caraway (Carum carvi L.), bitter orange (Citrus aurantium L.), bergamot orange (Citrus bergamia Risso & Poit), coriander (Coriandrum sativum L.), common juniper (Juniperus communis L.), English lavender (Lavandula angustifolia Mill.) corn mint (Mentha arvensis L.), pennyroyal (Mentha pulegium L.), basil (Ocimum basilicum L.), lemon basil (Ocimum citriodorum Vis), marjoram (O. majorana L.), oregano (O. vulgare L.), bay tree (Pimenta racemosa (Mill.) J.W. Moore), rosmary (Rosmarinus officinalis L.), common sage (Salvia officinalis L.), sage (Salvia sterea L.), tansy (Tanacetum vulgare L.), thyme (Thymus satureoides Coss. & Balansa., T. vulgaris L.) and ginger (Zingiber cassumunar Roxb.)||A. alternata, Stachybotrys chartarum, C. cladosporioides and A. niger||High antifungal activity|
The group of most effective essential oils including coriander, lemon basil, oregano, caraway, bay tree and thyme achieved high inhibition levels up to 100% across the entire spectrum of target pathogenic fungi
Moderate antifungal activity:
English lavender, pennyroyal, corn mint and sage exceeded 50% inhibitory effect boundary level in all target species except A. niger. Marjoram also did not exceed 50% inhibitory effect in C. cladosporioides
Low antifungal activity:
Bitter orange, bergamot orange, common juniper,, basil, common sage, tansy and ginger all failed to reach 50% antifungal inhibitive effect in a single target fungi
|Siberian fir (Abies sibirica L.), common caraway (Carum carvi L.), peppermint (Mentha piperita L.), willow-leaved gum tree (Eucalyptus globulus Labill.), lemon thyme (Thymus pulegioides L.), clove tree (S. aromaticum (Linn.) Merril & Perry) and bergamot orange (C. bergamia Risso & Poit)||The dominant species isolated from walls and air samples were A. versicolor, A. niger, A. fumigatus, Cladosporium sphaerospermum, C. cladosporioides, P. chrysogenum, P. aurantiogriseum, P. simplicissimum and||The highest fungicidal activity was demonstrated by clove oil. All cultures were affected and the fungicidal zones ranged from 20 to 50.5 mm. This fungicidal activity was comparable to the most effective disinfectant (Biosheen 20.9–57.5 mm). Next, fir oil was also effective against all fungi tested, but its fungicidal impact was less than that of clove oil||(34)|
|Ulocladium chartarum. In addition, the fungus Penicillium digitatum was found spreading on the wall in one case|
|Crude extract of glycoalkaloids from nightshade (Solanaceae) plants||Aspergillus, Penicillium, Coprinellus, Fusarium, Rhizoctonia and Stemphylium genera||The extract of glycoalkaloids from nightshade plants demonstrated only partial growth inhibition of Fusarium and Rhizoctonia||(35)|
|Essential oils from black peper (Piper nigrum Linn.), castor oil (Ricinus communis Linn.), cedar (Cedrus deodara (Roxb.) Loud.), clove (S. aromaticum Linn.), eucalyptus (Merrill & Perry E. globulus Labill.), bitter orange (C. aurantium Linn.), lemon (Citrus limon (Linn). Burm. f), olive (Olea europaea Linn.), and peppermint (M. piperita Linn.)||A. niger and Geotrichum candidum||Highest antifungal activity shown by clove, lemon, bitter orange and peppermint. The concentration of 5 ppm was as effectivity as 5 ppm Ketoconazole (positive control) and the lowest was shown by castor oil, cedar and olive||(36)|
|Thujopsene (found in the essential oil of a variety of conifers)||A. niger, Aspergillus ochraceus, A. sydowii, Aspergillus ustusa, Botrytis cinerea, Eurotium herbariorum, Gonytrichum macrocladum, Penicillium decumbensa, Penicillium expansum, Penicillium hirsutum, Penicillium polonicuma, Penicillium sp., Periconia britannicaa, Rhizopus stolonifer, S. chartarum and Ulocladium botrytisa||Thujopsene demonstrated fungicidal activity against only 5 of the 16 fungal strains tested||(37)|
|Cedar leaf oil (Thuja plicata)||Candida albicans and A. niger||C. albicans was readily killed by cedar leaf oil. A. niger was inhibited but complete eradication was not achieved||(38)|
|Essential oil extracts from manuka (Leptospermum scoparium) including eugenol, thymol, cinnamaldehyde, carvacrol, manuka oil, manuka oil less triketones fraction and triketones||Penicillium corylophilum, A. alternata and Cladosporium herbarum||Eugenol, cinnamaldehyde, thymol and carvacrol completely inhibited the growth of the three test fungi at a concentration of 1% w/v|
All the extracts, including eugenol, cinnamaldehyde and thymol virtually completely inhibited the growth of P. corylophilum on unfinished gypsum board at 3% w/v and significantly reduced growth on the finished gypsum boards
|Thyme essential oil and thymol||Aspergillus spp. A. versicolour, A. niger, A. sulphureus, A. flavus, P. chrysogenum, P. brevicompactum, P. griseofulvum, Penicillium spp., Alternaria spp., A. alternat, Ulocladium spp., Absidia spp., Mucor spp., C. spp., C. sphaerospermum, Trichoderma spp., Rhizopus spp., C. globosum, and S. chartarum||Both thymol and thyme essential oil showed strong fungicidal activity|
Vapor phase of the thyme essential oil at concentration of 82 μg L−1 exhibited fungi-static and/or fungicidal activity during 60 days of exposure in glass chambers. They were also demonstrated to be sporicidal against all tested mould species
|Essential oils from lemon (C. limon) including C. paradishi, C. sinensis, Citrus aurantifolia and Citrus reticulate||A. niger||C. aurantifolia and C. reticulata exhibited significant antifungal potency against building fungi||(41)|
|Volatile organic compounds (VOCs) produced from evaporating essential oils indoors lavender (L. angustifolis), eucalyptus (E. globulus) and tea tree (M. alternifolia)||Natural fungi contained within air samples||A slight decrease in fungal concentrations was observed in the first 30–60 min but levels quickly increased to pre-treatment concentrations||(23)|
|Essential oil from pine tree (Pinus sylvestris L.)||A. niger, Penicillium funiculosum, P. chrysogenum, T. viride, Ulocladium oudemansii, Paecilomyces variotii, Phoma glomerata, S. chartarum and A. versicolor||Pine oil displayed fungicidal activity against all fungi tested, although the effectiveness depended on the fungal species and the concentration of pine oil||(42)|
DMSO, Dimethyl sulfoxide; ATCC, American type culture collection.
Antifungal potential of essential oils for the control of indoor air environments
The biggest challenge when evaluating the antifungal potential of essential oils or their extracts (Table 1) is the lack of a standard method for both designing experiments and describing antifungal efficacy (43). The most commonly adopted screening method identified in the studies shown in Table 1 was the disk diffusion assay. This is where the essential oil or treatment is added to filter paper discs and placed in the centre of agar plates containing fungal lawn. The zone of clearing in fungal growth is measured as an indicator of fungal inhibition. Other studies also used modified versions of this method, including adding the essential oil through syringe injection or placing in a well in the centre of the agar plate (26), (36), (37). Rogawansamy et al. (15) used the disk diffusion assay in addition to a method adapted from Soylu et al. (44) to investigate the antifungal efficiency of the treatments in the vapour phase. Briefly, agar plates with fungal lawns are created and filter paper containing the treatment is placed on the inner surface of the agar plate lid, ensuring no direct contact with the fungal lawn. Plates are sealed with parafilm and antifungal efficiency is determined by measuring the zone of clearing. Another method frequently used was the serial dilution method, where serial dilutions of essential oils were prepared and inoculated with fungal cultures to determine the minimum concentration that inhibited fungal growth (25), (32), (40).
Even when the same method was used, it is difficult to compare results as a consequence of different reporting language used to describe antifungal efficacy. Using the disk diffusion assay, researchers reported the results as either diameter of zone of inhibition (15), (37) or as percentages of growth inhibition compared with the control plates (25), (29), (33). Using the serial dilution method, Šegvić Klarić et al. (40) reported antifungal efficacy using the term minimum inhibitory concentration (MIC), which is the lowest concentration that allowed no more than 20% fungal growth (determined by a reduction in the number of colonies in 10 μL of the dilution inoculated onto Sabouraud Glucose Agar incubated at 25°C for 7 days), and minimum fungicidal concentration (MFC), which was the lowest concentration of essential oil that completely inhibited the growth of the fungi. However, this differs from the definitions used by Stupar et al. (32), who also used a variation of the serial dilution method but reported the MIC as the lowest concentration without visible growth (assessed using a binocular microscope) and the MFC as the lowest concentration with no growth after inoculation of the original inoculum. This definition of MIC was supported by Verma et al. (45), who reported MIC as the lowest concentration that resulted in no growth after the incubation period.
The other challenge when evaluating the antifungal efficacy of essential oils is that most of the studies identified in Table 1 are laboratory based and there is a lack of in situ experiments within building environments. This makes it difficult to translate the experimental findings into ‘real-world’ recommendations. Only one study, by Su et al. (23), investigated the antifungal efficacy of essential oils by evaporating essential oil in indoor rooms and measuring the changes in air quality. Another four studies assessed the antifungal efficacy of essential oils against fungal growth on different types of wood surfaces used in building construction; however, all other studies identified were conducted on agar plates or broth cultures (36–39). There is clearly need for further research designed to investigate the antifungal efficacy in indoor environments (in situ) in order to validate the translation of laboratory-based outcomes. There is also a need to investigate the potential long-term persistence of the treatment and any optimum reapplication requirements in order to characterise antifungal capabilities.
Of the essential oils identified in Table 1, clove oil has been researched the most extensively, and there are a number of studies (laboratory and in situ) that have demonstrated that clove oil has strong antifungal capabilities. The most robust study demonstrated that clove essential oil had fungicidal activity comparable to commercial disinfectants and had the highest antifungal efficacy compared with Siberian fir, common caraway, peppermint, willow-leaved gum tree, lemon thyme and bergamot orange against fungi isolated from indoor air and surfaces (A. versicolor, A. niger, A. fumigatus, C. sphaerospermum, C. cladosporioides, P. chrysogenum, P. aurantiogriseum, P. simplicissimum, U. chartarum and P. digitatum) (34). Another study that was designed to have moderate transferability of results, by Yingprasert et al. (31), demonstrated that particle board that had been dipped in 0.63% clove oil completely inhibited Aspergillus and Trichothecium for up to 5 weeks. By increasing the concentration to 3%, it was found that Aspergillus and Trichothecium were inhibited for up to 9 weeks and the percentage of mass lost as a consequence of Trametes and Gloeophylum was reduced by 5% (31).
These findings were supported by other studies that used agar plates spiked with clove oil to demonstrate that it had higher antifungal efficacy against A. niger and G. candidum compared with black pepper, castor-oil plant, cedar, eucalyptus and olive (36). Also, a study using the agar spiked method found that clove oil was 100% effective at controlling R. chinensis, a common white rot fungi found in wood surfaces (29).
Tea tree oil
Two studies from Table 1 identify tea tree oil as a potential antifungal agent. The most translatable study was Su et al. (23), which evaluated tea tree oil by evaporating it in a room and measuring the changes in fungal concentration using an air sampler. This study is one of the few investigations into applying essential oils as a fungicide in a real-world building environment. It was found that the concentrations of fungi in the air initially decreased as a result of the VOCs from tea tree oil, but after 30–60 min, the concentrations returned to normal background indoor levels. However, one of the limitations of this study was that it did not compare the efficacy of tea tree oil to that of commercially available fungicides. Another study used the disk diffusion assay method to test tea tree oil against A. fumigatus and P. chrysogenum isolated from indoor air samples and found that it had greater fungicidal activity compared with some commercially available antifungal agents (15).
Oregano was identified as an effective antifungal agent in a study by Zabka et al. (33) using the agar microdilution method. It was demonstrated to have high inhibition levels against all fungi tested (A. alternata, S. chartarum, C. cladosporioidesand A. niger) and was more effective compared to other essential oils, including English lavender, pennyroyal, corn mint, sage, bitter orange, bergamot orange, common juniper, basil, common sage, tansy and ginger. However, this study used stock culture fungi, which makes it difficult to translate these results compared to studies using environmentally isolated fungi, and did not compare efficacy to that of commercially available fungicides. These findings were supported by another study that also used the microdilution methods to demonstrate that oregano displayed antifungal properties against A. fumigatus, A. nidulans, A. versicolor and a Penicillium species isolated from the frescoes within a monastery in Serbia. However, it was not as effective compared to the biocide benzalkonium chloride, a quaternary ammonium compound (32).
Thyme was also identified as an effective antifungal agent in a study by Zabka et al. (33), with greater fungal inhibition potential compared to essential oils from English lavender, pennyroyal, corn mint, sage, bitter orange, bergamot orange, common juniper, basil, common sage, tansy and ginger. However, this study used stock culture fungi, which makes it difficult to translate these results compared to studies using environmentally isolated fungi, and did not compare efficacy to that of commercially available fungicides. It was also demonstrated to have fungicidal and sporicidal activity in both the liquid and vapour phases against fungal isolates collected from the walls of damp buildings in Slovakia (40). However, in other more robust studies, it was shown to be not as effective compared to clove oil, fir oil or marjoram (28), (34).
Verma et al. (41) demonstrated that the volatile essential oils from lime (C. aurantifolia) and mandarin (C. reticulate) exhibited significant antifungal potency against building fungi A. niger. This was followed up by another study using a modified disk diffusion assay method (the essential oil was needle-inoculated in the centre of the agar plate), which showed that 5 ppm concentration of lemon essential oil was as effective as 5 ppm ketoconazole (a synthetic antifungal drug) against A. niger and G. candidum isolated from the surfaces and indoor air of buildings. The study also demonstrated essential oil from lemon to have greater antifungal potential compared to castor oil, cedar and olive (36).
Other essential oils demonstrating fungicidal potential
Other essential oils that demonstrated potential antifungal activity in at least one study (Table 1) include heartwood, marjoram, cinnamon, lemon basil, caraway, bay tree, fir, peppermint, pine, cedar leaf and essential oil extracts from manuka (eugenol, cinnamaldehyde, thymol and carvacrol).
Essential oils demonstrating only moderate or low fungicidal activity
The essential oils identified in Table 1 which demonstrate only moderate or limited antifungal activity include eucalyptus leaves, crêpe ginger, ginkgo leaves, myrrh, English lavender, pennyroyal, corn mint, sage, bitter orange, bergamot orange, common juniper, common basil, nightshade, castor-oil-plant, olive, willow-leaved gumtree and thujopsene (a compound found in the essential oil of a variety of conifers).
Mechanism of antifungal activity
Understanding the mechanism(s) of action of different antimicrobial agents is important to characterise efficacy as one agent may not inhibit all microorganisms. It is important to acknowledge the principal differences between bacteria and fungi. The structures of fungi and bacteria differ in significant ways, for example most fungi are diploid in nature and have longer generation time compared with bacteria (46). This means that antibacterial and antifungal agents target structures and functions most relevant to the organisms to be inhibited. For example, many antibacterial agents inhibit steps important for the formation of peptidoglycan (47), the essential component of the bacterial cell wall. In contrast, most antifungal compounds target either the formation or the function of ergosterol (48), (49) an important component of the fungal cell membrane. This membrane interaction weakens the structure, increasing permeability, which is responsible for the leakage of solutes across the membrane and causes cell lysis. For example, Shao et al. (50) described this mechanism of action when applying tea tree oil on B. cinerea (an important fungus in viticulture and food spoilage). Tea tree oil was found to inhibit the growth of the fungus and germination of spores was suppressed. The cell wall structure was reported to have lost its ultrastructure and showed thickening and rupturing. The authors concluded that the cell wall integrity was destroyed, increasing the membrane permeability.
Overall, there is currently limited knowledge regarding the antimicrobial mechanisms of essential oils, particularly with regards to antifungal activity (36), (49). A few authors have mentioned the antimicrobial activity of essential oils; however, the mechanism of action has not been studied in great detail (49), (51). Chemical analysis of essential oils show that the major active components are phenols, terpenes, aldehydes and ketones (52), and it is generally believed that essential oils principally act against cell cytoplasmic membranes of microorganisms. Hydrophobicity is an important characteristic of essential oils and their components (51), which may enable them to accumulate in cell membranes, disturbing the structures and causing an increase of permeability.
One study by Pinto et al. (49) demonstrated that clove oil and eugenol (the main component of many essential oils) was found to be fungicidal as a result of extensive lesion of the fungal cell membrane. In addition, clove oil and eugenol reduced the quantity of ergosterol, a specific fungal cell membrane component. This resulted in inhibition of germ tube formation of C. albicans (49). Similarly, it has been suggested that the antifungal action of tea tree oil is as a result of its capability to change or damage the function of fungal membranes (50), (53).
A great deal remains to be learned about the mechanisms of action of essential oils against fungal species. Although some progress has been made with clinical investigations, a greater understanding of these mechanisms is clearly lacking for other environmental organisms. Studies of the mechanisms of action relevant to fungal species in indoor air would allow more efficient and effective use of these agents.
Potential health effects – is ‘natural’ safer?
The increasing interest in ‘natural’ products for controlling microorganisms in indoor environments is due in part to the perception of benefit (i.e. inhibition of fungal growth) without the need for using potentially ‘harmful synthetic chemicals’. However, this assumption that ‘natural’ products are not harmful to human health is flawed.
Currently, there are limited studies investigating the potential adverse health consequences of repeated exposure to essential oils. The oils themselves are complex mixtures, which may contain naturally occurring contact sensitisers. In fact, some evidence suggests that they are potential skin allergens or sensitising agents (23), (54), (55). An ideal antifungal agent would not generate toxic fumes during application and is non-irritating if accidentally exposed to skin. Skin irritation and skin sensitisation are different responses; skin irritation occurs on the first exposure to the agent; the inflammatory reaction is typically rapid and the severity will depend on the concentration of the irritant present, compared with skin sensitisation, which is a complex allergic immunological response, with the reaction typically occurring after repeated exposure to the chemical and is usually irreversible (i.e. once sensitised, always react). Schaller and Korting (55) described a case report of allergic contact dermatitis due to repeated exposure to essential oil use in aromatherapy (applied topically or released as aerosols). There have also been several studies that have demonstrated exposure to essential oils exacerbated respiratory problems including asthma, decreased pulmonary function and increased chest tightness (56), (57).
Thus, the perception that ‘natural’ is safer may not necessarily be appropriate when considering essential oils for fungicidal treatment, and care must be taken with their repeated application in the indoor environment. Essential oils should be considered in the same way that use of chemical fungicides would be, based on risk assessment.
Conclusion and recommendations
Fungal contamination of indoor buildings and indoor air quality is a health issue of increasing concern. There is a need for greater guidance regarding appropriate antifungal agents to treat fungal contamination of buildings, as well as a drive from consumers and other groups to consider the potential of essential oils as a ‘natural’ alternative to commercially available fungicides. This review identifies the studies assessing the fungicidal potential of essential oils against fungi relevant to indoor air quality. The biggest challenge with comparing the fungicidal efficacy of essential oils from different studies is the lack of a standard method and reporting language. Additionally, the efficacy of essential oils is also dependant on the fungal species being challenged which makes it difficult to compare studies using different fungal isolates.
However, despite these challenges, clove oil was identified as the best-performing essential oil within the more robust studies. Additionally, there appears to be some evidence to support the essential oils tea tree oil, oregano, thyme and lemon as potential antifungal agents with relevance to indoor air quality. Heartwood, marjoram, cinnamon, lemon basil, caraway, bay tree, fir, peppermint, pine, cedar leaf and manuka were also identified in at least one study as having antifungal potential; however, there is a need for more robust studies to examine these further.
Future studies should focus on comparing the efficacy of these essential oils against a large number of fungal isolates from indoor environments. Studies will then need to focus on translating these results with in situ studies investigating the effectiveness in actual buildings and assessing the potential for long-term antifungal persistence. The studies identified in this review, which were either moderately or comparatively translational (23), (28), (31), (38), (39), (40), can inform the design of these studies. However, they should additionally compare the efficacy of essential oils to commercially available fungicides and examine the effect of time on fungicidal activity. Furthermore, when considering the application of these essential oils in building environments, the effect of different concentrations, mechanisms of application and the potential human side effects must also be examined.
Research funding: Authors state no funding involved. Conflict of interest: Authors have no conflicts of interest to declare. Informed consent: Informed consent is not applicable. Ethical approval: The conducted research is not related to either human or animal use.
1. Daisey JM, Angell WJ, Apte MG. Indoor air quality, ventilation and health symptoms in schools: an analysis of existing information. Indoor Air 2003;13(1):53–64.10.1034/j.1600-0668.2003.00153.xSearch in Google Scholar
2. Robbins CA, Swenson LJ, Nealley ML, Kelman BJ, Gots RE. Health effects of mycotoxins in indoor air: a critical review. Appl Occup Environ Hyg 2000;15(10):773–84.10.1080/10473220050129419Search in Google Scholar
4. Bird C, Balshaw S, Anderson W. Getting the best answer by asking the right question-case studies in occupational exposure to mould. J Health Saf Res Practice 2012;4:19–27.Search in Google Scholar
5. Arthur R. Damp Indoor Spaces and Health. Institute of Medicine: Committee on Damp Indoor Spaces and Health. Washington, DC, The National Academy Press, 2004: 355. ISBN 0-309-09193-4.Search in Google Scholar
8. Asher MI, Montefort S, Björkstén B, Lai CK, Strachan DP, et al. Worldwide time trends in the prevalence of symptoms of asthma, allergic rhinoconjunctivitis, and eczema in childhood: ISAAC Phases One and Three repeat multicountry cross-sectional surveys. Lancet 2006;368(9537):733–43.10.1016/S0140-6736(06)69283-0Search in Google Scholar
9. New York City Department of Health and Mental Hygiene. Guidelines on assessment and remediation of fungi in indoor environments. New York, USA: The New York City Department of Health and Mental Hygiene, 2008.Search in Google Scholar
10. Kim K-H, Jahan SA, Kabir E. A review on human health perspective of air pollution with respect to allergies and asthma. Environ Int 2013;59:41–52.10.1016/j.envint.2013.05.007Search in Google Scholar PubMed
11. Burr ML, Matthews IP, Arthur RA, Watson HL, Gregory CJ, et al. Effects on patients with asthma of eradicating visible indoor mould: a randomised controlled trial. Thorax 2007;62(9):767–72.10.1136/thx.2006.070847Search in Google Scholar PubMed PubMed Central
12. Cooley JD, Wong WC, Jumper CA, Straus DC. Correlation between the prevalence of certain fungi and sick building syndrome. Occup Environ Med 1998;55(9):579–84.10.1136/oem.55.9.579Search in Google Scholar PubMed PubMed Central
14. Hänninen OO. WHO guidelines for indoor air quality: dampness and mold. Fundamentals of mold growth in indoor environments and strategies for healthy living. Wageningen, Netherlands: Springer, 2011:277–302.Search in Google Scholar
15. Rogawansamy S, Gaskin S, Taylor M, Pisaniello D. An evaluation of antifungal agents for the treatment of fungal contamination in indoor air environments. Int J Environ Res Public Health 2015;12(6):6319–32.10.3390/ijerph120606319Search in Google Scholar PubMed PubMed Central
16. Chakravarty P, Kovar B. Engineering case report: evaluation of five antifungal agents used in remediation practices against six common indoor fungal species. J Occup Environ Hyg 2013;10(1):D11–6.10.1080/15459624.2012.740987Search in Google Scholar PubMed
17. Kemp P, Neumeister-Kemp H, Cheong C. Australian Mould Guideline. Osborne Park, Western Australia: Mycologia Australia Pty Ltd; 2005. ISBN: 9780980359404.Search in Google Scholar
18. Ogar A, Tylko G, Turnau K. Antifungal properties of silver nanoparticles against indoor mould growth. Sci Total Environ 2015;521:305–14.10.1016/j.scitotenv.2015.03.101Search in Google Scholar PubMed
19. Shoemaker RC, House DE. A time-series study of sick building syndrome: chronic, biotoxin-associated illness from exposure to water-damaged buildings. Neurotoxicol Teratol 2005;27(1):29–46.10.1016/j.ntt.2004.07.005Search in Google Scholar PubMed
20. Clausen CA, Yang VW. Mold inhibition on unseasoned southern pine. International research group on wood preservation. Stockholm, Sweden: IRG Secretariate, 2003:03-10465.Search in Google Scholar
22. Mehra T, Köberle M, Braunsdorf C, Mailänder-Sanchez D, Borelli C, et al. Alternative approaches to antifungal therapies. Exp Dermatol 2012;21(10):778–82.10.1111/exd.12004Search in Google Scholar PubMed PubMed Central
25. Al-Sabri AE, Moslem MA, Hadi S. Antifungal activity of Commiphora myrrha L. against some air fungi. J Pure Appl Microbiol 2015;8(5):3951–5.Search in Google Scholar
26. Ficker CE, Arnason J, Vindas P, Alvarez L, Akpagana K, et al. Inhibition of human pathogenic fungi by ethnobotanically selected plant extracts. Mycoses 2003;46(1–2):29–37.10.1046/j.1439-0507.2003.00838.xSearch in Google Scholar PubMed
27. Salem MZ, Zidan YE, El Hadidi NM, Mansour MM, Elgat WAA. Evaluation of usage three natural extracts applied to three commercial wood species against five common molds. Int Biodeterior Biodegradation 2016;110:206–26.10.1016/j.ibiod.2016.03.028Search in Google Scholar
28. So H-S, Jang H-S, Lee B-R, So S-Y. Antifungal performance of BFS mortar with various natural antifungal substances and their physical properties. Constr Build Materi 2016;108:154–62.10.1016/j.conbuildmat.2015.12.022Search in Google Scholar
29. Xie Y, Yang Z, Cao D, Rong F, Ding H, et al. Antitermitic and antifungal activities of eugenol and its congeners from the flower buds of Syzgium aromaticum (clove). Ind Crops Prod 2015;77:780–6.10.1016/j.indcrop.2015.09.044Search in Google Scholar
30. Yingprasert W, Matan N, Chaowana P. Fungal resistance and physico-mechanical properties of cinnamon oil and clove oil-treated rubberwood particleboards. J Trop For Sci 2015;27(1):69–79.Search in Google Scholar
31. Yingprasert W, Matan N, Matan N. Effects of surface treatment with cinnamon oil and clove oil on mold resistance and physical properties of rubberwood particleboards. Eur J Wood Wood Prod 2015;73(1):103–9.10.1007/s00107-014-0857-xSearch in Google Scholar
32. Stupar M, Grbić ML, Simić GS, Jelikić A, Vukojević J, et al. A sub-aerial biofilms investigation and new approach in biocide application in cultural heritage conservation: holy Virgin Church (Gradac Monastery, Serbia). Indoor Built Environ 2014;23(4):584–93.10.1177/1420326X12466753Search in Google Scholar
33. Zabka M, Pavela R, Prokinova E. Antifungal activity and chemical composition of twenty essential oils against significant indoor and outdoor toxigenic and aeroallergenic fungi. Chemosphere 2014;112:443–8.10.1016/j.chemosphere.2014.05.014Search in Google Scholar PubMed
34. Levinskaitė L, Paškevičius A. Fungi in water-damaged buildings of vilnius old city and their susceptibility towards disinfectants and essential oils. Indoor Built Environ 2013;22(5):766–75.10.1177/1420326X12458514Search in Google Scholar
35. Sasso S, Scrano L, Bonomo M, Salzano G, Bufo S. Secondary metabolites: applications on cultural heritage. Commun Agr Appl Biol Sci 2012;78(2):101–8.Search in Google Scholar
36. Verma RK, Chaurasia L, Kumar M. Antifungal activity of essential oils against selected building fungi. Indian J Nat Prod Resour 2011;2(4):448–51.Search in Google Scholar
37. Polizzi V, Fazzini L, Adams A, Picco AM, De Saeger S, et al. Autoregulatory properties of (+)-thujopsene and influence of environmental conditions on its production by Penicillium decumbens. Microb Ecol 2011;62(4):838.10.1007/s00248-011-9905-9Search in Google Scholar PubMed
38. Hudson J, Kuo M, Vimalanathan S. The antimicrobial properties of cedar leaf (Thuja plicata) oil; a safe and efficient decontamination agent for buildings. Int J Environ Res Public Health 2011;8(12):4477–87.10.3390/ijerph8124477Search in Google Scholar PubMed PubMed Central
40. Šegvić Klarić M, Kosalec I, Mastelić J, Piecková E, Pepeljnak S. Antifungal activity of thyme (Thymus vulgaris L.) essential oil and thymol against moulds from damp dwellings. Lett Appl Microbiol 2007;44(1):36–42.10.1111/j.1472-765X.2006.02032.xSearch in Google Scholar PubMed
41. Verma R, Chaurasia L, Katiyar S. Evaluation of antifungal potency of citrus essential oils against building fungi. Pestology 2007;31(1):29–31.Search in Google Scholar
42. Motiejūnaitė O, Dalia Pečiulytė D. Fungicidal properties of Pinus sylvestris L. for improvement of air quality. Medicina (Kaunas) 2004;8:787–94.Search in Google Scholar
43. Delespaul Q, de Billerbeck VG, Roques CG, Michel G, Marquier-Viñuales C, et al. The antifungal activity of essential oils as determined by different screening methods. J Essent Oil Res 2000;12(2):256–66.10.1080/10412905.2000.9699510Search in Google Scholar
44. Soylu EM, Kurt Ş, Soylu S. In vitro and in vivo antifungal activities of the essential oils of various plants against tomato grey mould disease agent Botrytis cinerea. Int J Food Microbiol 2010;143(3):183–9.10.1016/j.ijfoodmicro.2010.08.015Search in Google Scholar PubMed
45. Verma RK, Chaurasia L, Katiyar S. Evaluation of antifungal potency of citrus essential oils against building fungi. Pestology 2007:31(1):29–31.Search in Google Scholar
46. Ghannoum MA, Rice LB. Antifungal agents: mode of action, mechanisms of resistance, and correlation of these mechanisms with bacterial resistance. Clin Microbiol Rev 1999;12(4):501–17.10.1128/CMR.12.4.501Search in Google Scholar PubMed PubMed Central
49. Pinto E, Vale-Silva L, Cavaleiro C, Salgueiro L. Antifungal activity of the clove essential oil from Syzygium aromaticum on Candida, Aspergillus and dermatophyte species. J Med Microbiol 2009;58(11):1454–62.10.1099/jmm.0.010538-0Search in Google Scholar PubMed
50. Shao X, Cheng S, Wang H, Yu D, Mungai C. The possible mechanism of antifungal action of tea tree oil on Botrytis cinerea. J Appl Microbiol 2013;114(6):1642–9.10.1111/jam.12193Search in Google Scholar PubMed
51. Lv F, Liang H, Yuan Q, Li C. In vitro antimicrobial effects and mechanism of action of selected plant essential oil combinations against four food-related microorganisms. Food Res Int 2011;44(9):3057–64.10.1016/j.foodres.2011.07.030Search in Google Scholar
53. Huang R, Pyankov OV, Yu B, Agranovski IE. Inactivation of fungal spores collected on fibrous filters by Melaleuca alternifolia (tea tree oil). Aerosol Sci Technol 2010;44(4):262–8.10.1080/02786820903580188Search in Google Scholar
54. Lalko J, Api A. Investigation of the dermal sensitization potential of various essential oils in the local lymph node assay. Food Chem Toxicol 2006;44(5):739–46.10.1016/j.fct.2005.10.006Search in Google Scholar PubMed
55. Schaller M, Korting H. Allergie airborne contact dermatitis from essential oils used in aromatherapy. Clin Exp Dermatol 1995;20(2):143–5.10.1111/j.1365-2230.1995.tb02719.xSearch in Google Scholar PubMed
56. Galdi E, Perfetti L, Calcagno G, Marcotulli M, Moscato G. Exacerbation of asthma related to Eucalyptus pollens and to herb infusion containing Eucalyptus. Monaldi Arch Chest Dis 2002;59(3):220–1.Search in Google Scholar
57. Opiekun R, Smeets M, Sulewski M, Rogers R, Prasad N, et al. Assessment of ocular and nasal irritation in asthmatics resulting from fragrance exposure. Clin Exp Allergy 2003;33(9):1256–65.10.1046/j.1365-2222.2003.01753.xSearch in Google Scholar PubMed
©2018 Walter de Gruyter GmbH, Berlin/Boston