Review
Essential oils: their antibacterial properties and potential applications in foods—a review

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Abstract

In vitro studies have demonstrated antibacterial activity of essential oils (EOs) against Listeria monocytogenes, Salmonella typhimurium, Escherichia coli O157:H7, Shigella dysenteria, Bacillus cereus and Staphylococcus aureus at levels between 0.2 and 10 μl ml−1. Gram-negative organisms are slightly less susceptible than gram-positive bacteria. A number of EO components has been identified as effective antibacterials, e.g. carvacrol, thymol, eugenol, perillaldehyde, cinnamaldehyde and cinnamic acid, having minimum inhibitory concentrations (MICs) of 0.05–5 μl ml−1 in vitro. A higher concentration is needed to achieve the same effect in foods. Studies with fresh meat, meat products, fish, milk, dairy products, vegetables, fruit and cooked rice have shown that the concentration needed to achieve a significant antibacterial effect is around 0.5–20 μl g−1 in foods and about 0.1–10 μl ml−1 in solutions for washing fruit and vegetables. EOs comprise a large number of components and it is likely that their mode of action involves several targets in the bacterial cell. The hydrophobicity of EOs enables them to partition in the lipids of the cell membrane and mitochondria, rendering them permeable and leading to leakage of cell contents. Physical conditions that improve the action of EOs are low pH, low temperature and low oxygen levels. Synergism has been observed between carvacrol and its precursor p-cymene and between cinnamaldehyde and eugenol. Synergy between EO components and mild preservation methods has also been observed. Some EO components are legally registered flavourings in the EU and the USA. Undesirable organoleptic effects can be limited by careful selection of EOs according to the type of food.

Introduction

In spite of modern improvements in slaughter hygiene and food production techniques, food safety is an increasingly important public health issue (WHO, 2002a). It has been estimated that as many as 30% of people in industrialised countries suffer from a food borne disease each year and in 2000 at least two million people died from diarrhoeal disease worldwide (WHO, 2002a). There is therefore still a need for new methods of reducing or eliminating food borne pathogens, possibly in combination with existing methods (the hurdle principle; Leistner, 1978). At the same time, Western society appears to be experiencing a trend of ‘green’ consumerism Tuley de Silva, 1996, Smid and Gorris, 1999, desiring fewer synthetic food additives and products with a smaller impact on the environment. Furthermore, the World Health Organization has recently called for a worldwide reduction in the consumption of salt in order to reduce the incidence of cardio-vascular disease (WHO, 2002b). If the level of salt in processed foods is reduced, it is possible that other additives will be needed to maintain the safety of foods. There is therefore scope for new methods of making food safe which have a natural or ‘green’ image. One such possibility is the use of essential oils as antibacterial additives.

Essential oils (EOs) (also called volatile or ethereal oils; Guenther, 1948) are aromatic oily liquids obtained from plant material (flowers, buds, seeds, leaves, twigs, bark, herbs, wood, fruits and roots). They can be obtained by expression, fermentation, enfleurage or extraction but the method of steam distillation is most commonly used for commercial production of EOs (Van de Braak and Leijten, 1999). The term ‘essential oil’ is thought to derive from the name coined in the 16th century by the Swiss reformer of medicine, Paracelsus von Hohenheim; he named the effective component of a drug Quinta essentia (Guenther, 1948). An estimated 3000 EOs are known, of which about 300 are commercially important—destined chiefly for the flavours and fragrances market (Van de Braak and Leijten, 1999). It has long been recognised that some EOs have antimicrobial properties Guenther, 1948, Boyle, 1955 and these have been reviewed in the past Shelef, 1983, Nychas, 1995 as have the antimicrobial properties of spices (Shelef, 1983) but the relatively recent enhancement of interest in ‘green’ consumerism has lead to a renewal of scientific interest in these substances Nychas, 1995, Tuley de Silva, 1996. Besides antibacterial properties Deans and Ritchie, 1987, Carson et al., 1995a, Mourey and Canillac, 2002, EOs or their components have been shown to exhibit antiviral (Bishop, 1995), antimycotic Azzouz and Bullerman, 1982, Akgül and Kivanç, 1988, Jayashree and Subramanyam, 1999, Mari et al., 2003, antitoxigenic Akgül et al., 1991, Ultee and Smid, 2001, Juglal et al., 2002, antiparasitic Pandey et al., 2000, Pessoa et al., 2002, and insecticidal Konstantopoulou et al., 1992, Karpouhtsis et al., 1998 properties. These characteristics are possibly related to the function of these compounds in plants Guenther, 1948, Mahmoud and Croteau, 2002.

The purpose of this paper is to provide an overview of the published data on the antibacterial activity of those EOs and their components that could be considered suitable for application in or on foods, and to describe their possible modes of action. The current knowledge on potential antagonists and synergists is presented; legal and safety aspects are discussed and areas for future research are proposed. Although some data are presented on spoilage flora, this paper will focus chiefly on the antibacterial effect of EOs on food borne pathogens and, in particular, those for which food animals are the major reservoir.

Although spices have been used for their perfume, flavour and preservative properties since antiquity (Bauer et al., 2001), of the known EOs, only oil of turpentine was mentioned by Greek and Roman historians (Guenther, 1948). Distillation as a method of producing EOs was first used in the East (Egypt, India and Persia) (Guenther, 1948) more than 2000 years ago and was improved in the 9th century by the Arabs (Bauer et al., 2001). The first authentic written account of distillation of essential oil is ascribed to Villanova (ca. 1235–1311), a Catalan physician (Guenther, 1948). By the 13th century EOs were being made by pharmacies and their pharmacological effects were described in pharmacopoeias (Bauer et al., 2001) but their use does not appear to have been widespread in Europe until the 16th century, from which time they were traded in the City of London (Crosthwaite, 1998). Publishing separately in that century on the distillation and use of EOs, two Strassburg physicians, Brunschwig and Reiff, mention only a relatively small number of oils between them; turpentine, juniper wood, rosemary, spike (lavender), clove, mace, nutmeg, anise and cinnamon (Guenther, 1948). According to the French physician, Du Chesne (Quercetanus), in the 17th century the preparation of EOs was well known and pharmacies generally stocked 15–20 different oils (Guenther, 1948). The use of tea tree oil for medical purposes has been documented since the colonisation of Australia at the end of the 18th century, although it is likely to have been used by the native Australians before that (Carson and Riley, 1993). The first experimental measurement of the bactericidal properties of the vapours of EO is said to have been carried out by De la Croix in 1881 (Boyle, 1955). However, in the course of the 19th and 20th centuries the use of EOs in medicine gradually became secondary to their use for flavour and aroma (Guenther, 1948).

The greatest use of EOs in the European Union (EU) is in food (as flavourings), perfumes (fragrances and aftershaves) and pharmaceuticals (for their functional properties) Bauer and Garbe, 1985, Van Welie, 1997, Van de Braak and Leijten, 1999. The well-known use of EO in aromatherapy constitutes little more than 2% of the total market (Van de Braak and Leijten, 1999). Individual components of EOs are also used as food flavourings, either extracted from plant material or synthetically manufactured (Oosterhaven et al., 1995).

The antibacterial properties of essential oils and their components are exploited in such diverse commercial products as dental root canal sealers (Manabe et al., 1987), antiseptics Bauer and Garbe, 1985, Cox et al., 2000 and feed supplements for lactating sows and weaned piglets Van Krimpen and Binnendijk, 2001, Ilsley et al., 2002. A few preservatives containing EOs are already commercially available. ‘DMC Base Natural’ is a food preservative produced by DOMCA S.A., Alhendı́n, Granada, Spain and comprises 50% essential oils from rosemary, sage and citrus and 50% glycerol (Mendoza-Yepes et al., 1997). ‘Protecta One’ and ‘Protecta Two’ are blended herb extracts produced by Bavaria Corp. Apopka, FL, USA and are classed as generally recognized as safe (GRAS) food additives in the US. Although the precise contents are not made known by the manufacturer, the extracts probably contain one or more EOs and are dispersed in solutions of sodium citrate and sodium chloride, respectively (Cutter, 2000). Further physiological effects of EOs are made use of in widely differing products such as commercial potato sprout suppressants (Hartmans et al., 1995) and insect repellents (Carson and Riley, 1993).

Section snippets

Composition of EOs

Steam distillation is the most commonly used method for producing EOs on a commercial basis. Extraction by means of liquid carbon dioxide under low temperature and high pressure produces a more natural organoleptic profile but is much more expensive (Moyler, 1998). The difference in organoleptic profile indicates a difference in the composition of oils obtained by solvent extraction as opposed to distillation and this may also influence antimicrobial properties. This would appear to be

In vitro tests of antibacterial activity

Tests of antimicrobial activity can be classified as diffusion, dilution or bioautographic methods (Rios et al., 1988). The principles and practice of these test methods are explained in the literature Barry, 1976, Davidson and Parish, 1989, Hodges and Hanlon, 1991 but it appears that no standardised test has been developed for evaluating the antibacterial activity of possible preservatives against food-related microorganisms, although the need for such has been indicated (Davidson and Parish,

Tests of antibacterial activity of EOs in food systems

Although, as mentioned previously, a small number of food preservatives containing EOs is commercially available, until the early 1990s very few studies of the activity of EOs in foods had been published (Board and Gould, 1991). Since then a fair number of trials have been carried out with EOs in foods. An overview of the literature reporting studies on the antibacterial effect of EOs or their components in foods is presented in Table 6. Reports of studies using diluted foods or food slurries

Mode of antibacterial action

Although the antimicrobial properties of essential oils and their components have been reviewed in the past Koedam, 1977a, Koedam, 1977b, Shelef, 1983, Nychas, 1995, the mechanism of action has not been studied in great detail (Lambert et al., 2001). Considering the large number of different groups of chemical compounds present in EOs, it is most likely that their antibacterial activity is not attributable to one specific mechanism but that there are several targets in the cell Skandamis et

Susceptibility of gram-negative and gram-positive organisms

Most studies investigating the action of whole EOs against food spoilage organisms and food borne pathogens agree that, generally, EOs are slightly more active against gram-positive than gram-negative bacteria Shelef, 1983, Shelef et al., 1984, Farag et al., 1989, Mendoza-Yepes et al., 1997, Ouattara et al., 1997, Ouattara et al., 2001, Smith-Palmer et al., 1998, Marino et al., 1999, Marino et al., 2001, Negi et al., 1999, Juliano et al., 2000, Ruberto et al., 2000, Senatore et al., 2000,

Synergism and antagonism between components of EOs

The inherent activity of an oil can be expected to relate to the chemical configuration of the components, the proportions in which they are present and to interactions between them Dorman and Deans, 2000, Marino et al., 2001, Delaquis et al., 2002. An additive effect is observed when the combined effect is equal to the sum of the individual effects. Antagonism is observed when the effect of one or both compounds is less when they are applied together than when individually applied. Synergism

Synergism and antagonism between EO components and food preservatives or preservation methods

A number of potential synergists have been suggested for use with EOs: low pH, low water activity, chelators, low oxygen tension, mild heat and raised pressure, although not all of these have been researched in foodstuffs (Gould, 1996). This section will summarise studies on the combined effect of EOs or their components with the food additives sodium chloride, sodium nitrite and nisin and with preservation techniques of mild heat treatment, high hydrostatic pressure and anaerobic packaging.

Legal aspects of the use of EOs and their components in foods

A number of EO components have been registered by the European Commission for use as flavourings in foodstuffs. The flavourings registered are considered to present no risk to the health of the consumer and include amongst others carvacrol, carvone, cinnamaldehyde, citral, p-cymene, eugenol, limonene, menthol and thymol. Estragole and methyl eugenol were deleted from the list in 2001 due to their being genotoxic (Commission Decision of 23 January, 2002). New flavourings may only be evaluated

Safety data

In spite of the fact that a considerable number of EO components are GRAS and/or approved food flavourings, some research data indicate irritation and toxicity. For example, eugenol, menthol and thymol, when applied in root canal treatments, have been known to cause irritation of mouth tissues. The results of a cytotoxicity study on these compounds suggest that gum irritation may be related to membrane lysis and surface activity and that tissue penetration may be related at least partly to

Organoleptic aspects

If EOs were to be more widely applied as antibacterials in foods, the organoleptic impact would be important. Foods generally associated with herbs, spices or seasonings would be the least affected by this phenomenon and information on the flavour impact of oregano EO in meat and fish supports this. The flavour of beef fillets treated with 0.8% v/w oregano oil was found to be acceptable after storage at 5 °C and cooking (Tsigarida et al., 2000). The flavour, odour and colour of minced beef

Future perspectives

Arguably the most interesting area of application for EOs is the inhibition of growth and reduction in numbers of the more serious food borne pathogens such as Salmonella spp., E. coli O157:H7 and L. monocytogenes. The delay of spoilage and improvement of organoleptic qualities in vacuum packed meat or fish may also be interesting from a commercial point of view. In view of their organoleptic properties, EOs could most readily be incorporated in manufactured foods that are traditionally

Areas for future research

The action of EO components on proteins embedded in the cytoplasmic membrane and on phospholipids in the membrane is not yet fully identified and is a focal area for future research. Further elucidation of these mechanisms would provide insights that may prove useful for technological applications.

The antibacterial activity against bacterial cells in the stationary phase is a particularly appropriate subject for study (Rees et al., 1995). The extent to which bacteria can adapt to the presence

Conclusion

A number of EOs and several of their individual components exhibit antibacterial activity against food borne pathogens in vitro and, to a lesser extent, in foods. The phenolic components are most active and appear to act principally as membrane permeabilisers. Gram-positive organisms are generally more sensitive to EOs than gram-negative organisms. Undesirable organoleptic effects can be limited by careful selection of EO according to the type of food. Synergism and antagonism between

Acknowledgements

I thank Professor H.P. Haagsman, Dr. J.H. Houben and Dr. J.M.A. Snijders for their valuable comments on the manuscript and P.P. Deley for drawing the figures.

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