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Vapour phase a potential future use for essential oils as

  1. 1. UNDER THE MICROSCOPE Vapour phase: a potential future use for essential oils as antimicrobials? K. Laird1 and C. Phillips2 1 The Leicester School of Pharmacy, Faculty of Health and Life Sciences, Hawthorn Building, De Montfort University, Leicester, UK 2 School of Health, University of Northampton, Northampton, UK Introduction Essential oils (EOs) are extracts of plants prepared by steam distillation and are generally composed of a mix- ture of terpenes, terpiniods, aldehydes and alcohols, many of which are volatile. Their antimicrobial effects are well known and have been reviewed previously by Burt (2004) and Bakkali et al. (2008). The main disadvantage of using EOs in liquid phase is that generally they are more effec- tive antimicrobials when tested in culture than when tested, for example, in food systems, and so higher con- centrations are required to bring about the same effect. The components of EOs and their relative volatilities determine the characteristics of their vapours, which in turn has an effect on the antimicrobial potential (Burt 2004; Tullio et al. 2007). Recently, there have been studies confirming that vapour phases of EOs are more effective antimicrobials than their liquid phases including Eucalyp- tus globulus EO (Inouye et al. 2003; Tyagi and Malik 2011a), Melaleuca alternifolia (Mondello et al. 2009) lemon grass EO (Tyagi and Malik 2010b,c), and a range of others including thyme, fennel and lavender EOs (Soy- lu et al. 2006; Tullio et al. 2007). One of the reasons that has been suggested for the vapour phase being more effective is that the lipophilic molecules in the aqueous phase associate to form micelles and thus suppress that attachment of the EOs to the organism, whereas the vapour phase allows free attachment (Inouye et al. 2003). However, compared with the wealth of evidence for the effectiveness of EOs in liquid phase, the potential of EO vapours is relatively less researched, although gaining interest. Historical uses of vapours Inhalation of EO vapours in the form of smoke produced by bay leaves was apparently responsible for visions that came to the oracle at Delphi (Thompson 2003). The first record of EOs having medicinal uses was by Theopharu- stus in 4th century bc when they were used as antidotes to poisons and inhaled in vapour form to ease the throat. The use of EOs and EO vapours as a cure to be either consumed or inhaled before eating for nausea and stom- ach cramps caused by food consumption was suggested by Pliny in 23–72 ad (Arias and Ramon-Laca 2005). EO vapours were also used by the ancient Egyptians for med- icine, perfumery and spiritual life (Edris 2007). The first mention of EOs in the pharmacopeia was in the 13th Keywords antimicrobial, essential oils, vapours. Correspondence Katie Laird, The Leicester School of Pharmacy, Faculty of Health and Life Sciences, Hawthorn Building, De Montfort University, Leicester LE1 9BH, UK. E-mail: 2011 ⁄ 1843: received 28 October 2011, revised 25 November 2011 and accepted 25 November 2011 doi:10.1111/j.1472-765X.2011.03190.x Abstract Essential oil (EO) vapours have been known for their antimicrobial properties since the 4th century B.C.; however, it was not until the early 1960s that research into the potential of these volatile oils was explored. More recently, the use of EOs such as tea tree, bergamot, lavender and eucalyptus in vapour form has been shown to have antimicrobial effects against both bacteria and fungi, with range of methods being developed for dispersal and efficacy testing. To date, many applications for EO vapours as antimicrobials have been identi- fied including in the food and clinical arenas. Letters in Applied Microbiology ISSN 0266-8254 ª 2011 The Authors Letters in Applied Microbiology 54, 169–174 ª 2011 The Society for Applied Microbiology 169
  2. 2. century although generally in Europe, EOs were not used for medicinal purposes until the 16th century (Burt 2004), whilst in recent history, the first report of antimi- crobial activity from EO vapours was in 1960 (Maruzzella and Sicurella 1960). Screening methods The antimicrobial effect of EO vapours is usually assessed by an initial in vitro screening, and two main methods are used. The first is an adapted disc diffusion method, which was first used in the late 1950s, where the EO impregnated filter disc is placed on the lid of the petri dish and then zones of inhibition measured (Maruzzella and Sicurella 1960). However, it was another 40 years before it was fully described and utilized as a standardized method for the screening of EO vapours (Lopez et al. 2005). Although the method has been adapted in numer- ous ways in the last decade, for instance using a piece of enamel in the lid of the petri dish as a platform on which to place the impregnated disc (Mondello et al. 2009), all are based on the same principle. In the second method, for example, that used by Ino- uye et al. (2001), the EO and micro-organisms are placed separately into a sealed environment such as a jar which means that several organisms can be tested for suscepti- bility to one EO vapour at one time although the amount of EO used may be large, making it not a very cost-effec- tive method. However, it can also be used for the assess- ment of inhibitory effect on organisms inoculated onto surfaces and in air (Doran et al. 2009; Fisher et al. 2009; Laird et al. 2011). Recently, another adaptation of the disc diffusion method using a four sectioned petri dish has been pro- posed which, the authors claim, provides a more uniform headspace and reduces the costs both in terms of materi- als and labour (Kloucek et al. 2011). With this method, 36 petri dishes are required to test one EO vapour against six micro-organisms at six concentrations as compared with 108 petri dishes if using the disc volatilization method. Minimum inhibitory dose (MID), where the minimum dose of the vapour to inhibit growth is determined, is a parallel method to the MIC for EO liquids. This is gener- ally carried out in a sealed container, and the EO can either be placed on the container surface (slow evapora- tion) or as an impregnated disc (quick evaporation) (Ino- uye et al. 2003; Fisher and Phillips 2006). Many authors have calculated MID by dividing the dose of EO by the volume of air in the petri dish, which is relatively inaccu- rate because of the different volatilities of EO constitu- ents. As in this method the EO is applied to a small area such as a paper disc, the resulting inhibition zone is not only a measure of activity but also of the speed of evapo- ration of EO active components, which is also dependant on temperature. In one study that assessed the contribu- tion of vapours to the antimicrobial effect in the direct disc diffusion method, only the water-soluble components diffused across the agar whilst the redeposition of the vapourized components on the surface of the agar accounted for the remainder of the inhibition. For oils containing alcohols, ketones, esters, oxides and hydrocar- bons, the major inhibition came from the vapours, whereas for oils containing greater volumes of aldehydes, inhibition came from diffusion (Inouye et al. 2006). The other factor to be considered is that loss of vapour can occur through absorption into the media as chamber leakage and also spontaneous decomposition can occur (Inouye et al. 2001). Dispensing methods Dispersion other than by natural evaporation is an issue when considering the antimicrobial effect of EOs in vapour phase. The heating of EOs can increase the evapo- ration rate of the oils but can also destroy or alter some of the components and thus possibly affect the antimicro- bial effect of the oils (Su et al. 2007). When 15 EOs were dispersed using a heated aroma lamp and assessed for their volatile components, it was found that those vola- tiles trapped in the headspace of the aroma lamp had altered from being mainly monoterpene hydrocarbons (high volatility) to low volatility monoterpene alcohols and sesquiterpenes (Oberhofer et al. 1999). The incorpo- ration of oils into candles as a means of dispersion (Su et al. 2007) has a different effect than that of merely heat- ing the oils as it is proposed that the ionized vapour molecules have a greater attachment to the bacterial cell membrane, increasing permeability and hence cell death as shown by the enhancement of antibacterial activity of b-pinene vapour against Escherichia coli when the vapour is combined with an ionizing source such as a corona discharge or a candle flame (Gaunt et al. 2005). The use of water is not a very effective method for the dispersion of EOs or their vapours because phenolic com- pounds have poor solubility resulting in a reduced anti- microbial activity. Water also reduces volatility as compounds with hydroxyl groups may be more solvated and remain in water phase (Sato et al. 2006). Other dispersion methods have been tested. For exam- ple, when a room diffuser was used to dispense EO com- ponents linalool and carvacrol into the air, there was a reduction in bacterial counts 5 h after spraying (Krist et al. 2008). A 80% reduction in airborne bacteria was reported when an EO blend of geranium and lemongrass was dispersed continuously for 20 h via a fragrance Essential oil vapours and their antimicrobial activity K. Laird and C. Phillips 170 Letters in Applied Microbiology 54, 169–174 ª 2011 The Society for Applied Microbiology ª 2011 The Authors
  3. 3. generator working at 100% dispersing the EO vapour via negative and venturi airflow and without heat, although when output was reduced to 30% airborne counts increased and when exposure discontinued counts returned slowly to normal (Doran et al. 2009), indicating that continuous dispersion is necessary for total effective- ness. A similar conclusion can be made from the results of an investigation of the effect of evaporating EOs (lavender, eucalyptus and tea tree) on indoor air quality, although it was demonstrated that the emissions of the volatile organic compounds occurred within the first 20 min and lowest levels of airborne bacteria occurred at 30 min, after this time bacterial counts increased (Su et al. 2007). Toxicity There is limited published research on the toxicity of EO vapours per se; however, in the future this needs to be explored before they can be utilized as commercial antimi- crobials. As EOs are complex blends of components, indi- vidual volatile compounds need to be assessed as potential allergens. Currently, the European Flavour and Fragrance Association (EFFA) lists 24 allergens associated with EOs; however, these are all based on skin contact and not inha- lation (EFFA, 2011). A study assessing the vapours of five EOs of rose, lemon, rosemary and tea tree oil (TTO) showed that benzene, a known carcinogen, was released into the air, but the concentrations were significantly lower than the acute adverse concentrations of 7Æ6 ppm (Chiu et al. 2009). Patients with hypersensitivity who have been exposed perfume either through the airways or through eye exposure at 5 min intervals for a total of 30 min have shown increased dyspnea, coughing and eye irritation compared with the placebo group (Millqvist et al. 1999). It should be noted that volatile components such as terpenes, d-limonene, hydrocarbons, alcohols and ethers can play a role in the formation of secondary aerosols from interaction with oxidants, such as ozone, hydroxyl and nitrate radicals and form pollutants such as formal- dehyde (Su et al. 2007). Studies have shown that the vola- tile monoterpenes of the EOs, which have at least one unsaturated carbon–carbon bond can react with oxidants such as ozone, hydroxyl and nitrate radicals. This can result in the formation of chemicals like formaldehyde, thus creating secondary pollutants (Su et al. 2007) in addition to the oxidation of limonene and linalool which can form high molecular weight oxidation products such as aldehydes, ketones and organic acids. In vitro effects against bacteria An extensive study by Nedorostova et al. (2009) investi- gating the effect of 27 EO vapours against five food-borne pathogens (E. coli, Listeria monocytogenes, Salmonella ente- riditis, Staphylococcus aureus and Pseudomonas aeruginosa) using the disc volatilization method found that 13 had some antibacterial activity against at least one strain with the best results being produced by Armoracia rusticana that was active against all five pathogens at a concentra- tion of 0Æ0083 ll cm)3 . Several EO vapours including Mentha arvensis, Mentha piperita and Cymbopogon citratus are effective against Pseudomonas fluorescens reducing cell viability by 65–80% over 12-h exposure, which is enhanced using a combina- tion of EO vapours and negative air ions (NAI) with M. arvensis and NAI producing a 100% reduction in via- bility in 8 h (Tyagi and Malik 2010a). Mentha piperita vapour itself shows activity against a range of bacteria including E. coli isolates, Pseudomonas sp, Bacillus subtilis and Staph. aureus with zones of inhibi- tion varying between 22 mm for Ps. fluorescens to 35 mm for B. subtilis. In time-kill assays, 100% reduction in via- bility of B. subtilis occurs over 8 h, whereas for E. coli and Pseudomonas sp., only 74–85% reduction in viability occurs after 12 h (Tyagi and Malik 2011a). A similar study by the same authors testing E. globulus EO vapour also demonstrated that B. subtilis was the most susceptible of the bacteria tested with a 100% reduction in viability after 8 h compared with 80% reduction after 12 h for the other bacteria (Tyagi and Malik 2011a). If mixtures of EOs in vapour phase are used as antimi- crobials, there may either be an antagonistic effect or syn- ergistic effect, measured by assessment of the fractional inhibitory concentration index (FIC). For example, when cinnamon and clove EO vapours are combined, they exert an antagonistic effect against E. coli but a synergistic effect on a range of other bacteria such as L. monocytogenes and Yersinia enterolytica (Gon˜i et al. 2009). Morphological changes have been reported in a num- ber of studies investigating the effect of EO vapours on bacteria. Total deformation of Ps. fluorescens is brought about by Cymbopogon citrates EO vapour (Tyagi and Malik 2010b), whilst B. subtilis cells show complete degra- dation after exposure to M. piperita EO vapour (Tyagi and Malik 2011a). When Enterococcus sp. are treated with a citrus EO vapour, morphological changes also occur, together with a reduction in membrane potential, increase in cell perme- ability, loss of intracellular ATP and a decrease in intracel- lular pH (Fisher and Phillips 2009). This decrease in intracellular ATP and pH effect of an EO vapour corre- sponds to similar results for E. coli O157 and L. monocyt- ogenes when treated with several EOs (oregano, Chinese cinnamon and savoury) in liquid phase (Oussalah et al. 2007) although this does not necessarily mean that the liquid and vapour phases act by the same mechanism. K. Laird and C. Phillips Essential oil vapours and their antimicrobial activity ª 2011 The Authors Letters in Applied Microbiology 54, 169–174 ª 2011 The Society for Applied Microbiology 171
  4. 4. In vitro antifungal effects of EO vapours Cinnamon, clove, basil and ginger EO vapours have been shown to be effective against Aspergillus flavus and Peni- cillium islandicum (Lopez et al. 2005) and thyme, sage and nutmeg EO vapours against a range of Aspergillus sp. clinical isolates and environmental isolates of Penicillium sp. (Tullio et al. 2007) in vitro. Interestingly, although lemongrass is generally regarded as a very active antimicrobial, it does not suppress sporu- lation of a number of fungi such as Aspergillus fumigatus, Fusarium solani, Penicillium expansum or Rhizopus oryzae, whereas lavender and thyme EO vapours do have an antisporulating effect (Inouye et al. 1998) as does a mix- ture of orange and bergamot EOs in vapour phase (Phillips et al. 2011). Also being effective against bacteria, M. piperita vapour completely inhibits growth of a range of fungi and yeasts including Aspergillus sp. and Penicillium sp. both in the disc diffusion and time-kill assays (Tyagi and Malik 2011a), and E. globulus EO in vapour phase shows a simi- lar pattern of activity (Tyagi and Malik 2011a). Lemongrass vapour-treated Candida albicans shows complete degradation under SEM, whilst Atomic Force Microscope (AFM) shows a decrease in ‘roughness’ and TEM extensive internal damage with a distorted plasma- lemma and a dense cytoplasm, with liquid globules (Tyagi and Malik 2010b). Similar morphological changes such as cytoplasm coagulation, vacuolation, protoplast leakage and hyphal shrinking are seen in fungi treated with a range of EO vapours including thyme, fennel and laven- der (Soylu et al. 2006). From a study of the inhibition of apical growth of A. fumigatus by a number of EO vapours, it has been suggested that the effects are because of the direct accu- mulation of the vapours on mycelia. The fungistatic effect of some EO vapours such as lavender EO and TTO is therefore brought about by the selective inser- tion of components into the lipid-rich portion of the cell membrane disrupting membrane function, whilst the fungicidal effect of lemongrass EO vapour with aldehydes as its main components acts irreversibly by a cross linkage reaction within the cell membrane (Inouye et al. 2000). Use in food The use of EO vapours in food relates to their antimicro- bial nature against both food pathogens and also food spoilage organisms, particularly fungal species. One advantage is that in vapour phase, the components are dispersed and tend not to affect the organoleptic proper- ties of the food stuff to such an extent as EO liquids (Gon˜i et al. 2009). As little as 45-s exposure is required to reduce Enterococcus sp. by 4 log CFU g)1 on lettuce by a citrus EO vapour and sensory evaluation by an untrained panel indicated that the organoleptic properties of the foodstuff was not affected (Fisher et al. 2009). However, like EOs in liquid phase, vapours are less effective on food than in vitro. For example, thyme EO vapour completely eliminates Alternaria alternate growth in vitro but only reduces growth on cherry tomatoes (Feng et al. 2011). Similar results have been reported for a citrus EO vapour against A. alternate. In vitro growth is completely inhibited, but this is not the case when tested on tomatoes (Phillips et al. 2011). In the case of anthrac- nose rot produced by Colletotrichum coccodes (Wallr), a common cause of spoilage in tomatoes Origanum vulgare EO vapour is more effective in reducing spore germina- tion on tomatoes than in vitro. Lesions are suppressed although fruit cracking occurs which reduces the useful- ness of this treatment for food producers (Tzortzakis 2010). The assessment of the vapours of eucalyptus and cinna- mon EOs against postharvest pathogens on fresh produce (strawberries and tomatoes) demonstrated that after 8-h exposure and subsequent transfer to ambient temperature, the fruits maintained a low severity of decay; however, the organoleptic properties of the foodstuff were adversely affected (Tzortzakis 2007). In a study of ten EOs in vapour phase for their activity against rye bread spoilage fungi, mustard and lemongrass were the most effective with no growth after 14 days of any of the five fungi on rye bread when exposed to these vapours (Suhr and Nieisen 2003). The results of a study by Paparella et al. (2008) using flow cytometry to assess damage caused by EOs suggested that there may be a subpopulation of cells (in this case L. monocytogenes treated with thyme, oregano and cinna- mon EOs) that are sublethally damaged and are therefore able to recover, an important issue for food microbiolo- gists when designing processing procedures. Although this study was concerned with EOs in liquid phase, the possi- bility remains for vapour-treated cells and this is an area that requires exploration. Use in clinical environment Methicillin Resistant Staphylococcus aureus (MRSA) is an important pathogen in the clinical environment and has been found to be reduced by a treatment consisting of a grapefruit extract called CitricidalÔ combined with gera- nium or TTO in vapour form (Edwards-Jones et al. 2004) and a lemongrass and geranium EO vapour mixture (Bio- scentÔ) in vitro. The latter, it was suggested, could reduce also airborne contamination (Doran et al. 2009). Essential oil vapours and their antimicrobial activity K. Laird and C. Phillips 172 Letters in Applied Microbiology 54, 169–174 ª 2011 The Society for Applied Microbiology ª 2011 The Authors
  5. 5. In a hospital environment, the formation of bioflims is an important route for cross-contamination, and there- fore, a treatment that is environmentally friendly and effective in the removal and prevention of biofilms could provide a method of reducing hospital infections. A citrus EO vapour reduces the formation of biofilms by MRSA and methicillin Susceptible Staphylococcus aureus (MSSA) and also removes the biofilms once they are formed and, although it does not prevent the formation of vancomy- cin Resistant Enterococcus sp. (VRE) biofilms, it does remove them once formed (Laird et al. 2011). In an extensive study (Inouye et al. 2001) investigating the antibacterial effect of 14 EOs in vapour phase against four respiratory pathogens, Haemophilus influenzae was the most susceptible followed by Streptococcus pneumoniae and Streptococcus pyogenes and Staph. aureus. High vapour concentrations for short periods (1–2 h) were the most effective method of delivering the antibacterial effect, and thyme, lemongrass and cinnamon bark EO vapours were the most effective with the lowest MIDs at <12Æ5 mg l)1 air compared with, for example, 50 mg l)1 air for TTO and lavender. Conclusion There is growing evidence that EOs in vapour phase are effective antimicrobial systems and that they do have advantages over the use of EOs in liquid phase such as an increase in activity, use at lower concentrations, ability to be used in a range of environments, for example, as air decontaminants and, because of their volatility, the lack of changes to sensory properties of foodstuffs. However, there is not a general consistency concerning which EO in vapour phase will be effective against which type of micro-organism, and so the spectrum of activity of each EO vapour needs to be identified experimentally. 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