Essential Oils: Sources of Antimicrobials and Food Preservatives

Pandey, Abhay K.; Kumar, Pradeep; Singh, Pooja; Tripathi, Nijendra N.; Bajpai, Vivek K.

doi:10.3389/fmicb.2016.02161

MINI REVIEW article

Front. Microbiol., 16 January 2017

Sec. Microbiotechnology

Volume 7 - 2016 | https://doi.org/10.3389/fmicb.2016.02161

This article is part of the Research Topic Microbial Secondary Metabolites: Recent Developments and Technological Challenges View all 26 articles

Essential Oils: Sources of Antimicrobials and Food Preservatives

$\r\nAbhay K. Pandey$ Abhay K. Pandey¹

Pradeep Kumar²^*

Pooja Singh¹^*

Nijendra N. Tripathi¹

Vivek K. Bajpai³^*

¹Bacteriology and Natural Pesticide Laboratory, Department of Botany, Deen Dayal Upadhyay Gorakhpur University, Gorakhpur, India
²Department of Forestry, North Eastern Regional Institute of Science and Technology, Nirjuli, India
³Department of Applied Microbiology and Biotechnology, School of Biotechnology, Yeungnam University, Gyeongsan, South Korea

Aromatic and medicinal plants produce essential oils in the form of secondary metabolites. These essential oils can be used in diverse applications in food, perfume, and cosmetic industries. The use of essential oils as antimicrobials and food preservative agents is of concern because of several reported side effects of synthetic oils. Essential oils have the potential to be used as a food preservative for cereals, grains, pulses, fruits, and vegetables. In this review, we briefly describe the results in relevant literature and summarize the uses of essential oils with special emphasis on their antibacterial, bactericidal, antifungal, fungicidal, and food preservative properties. Essential oils have pronounced antimicrobial and food preservative properties because they consist of a variety of active constituents (e.g., terpenes, terpenoids, carotenoids, coumarins, curcumins) that have great significance in the food industry. Thus, the various properties of essential oils offer the possibility of using natural, safe, eco-friendly, cost-effective, renewable, and easily biodegradable antimicrobials for food commodity preservation in the near future.

Introduction

Since ancient times, commercial antimicrobial agents have been applied as a way to manage food deterioration or contamination. Nowadays, user concerns toward synthetic preservatives have resulted in increasing attention on various natural antimicrobials such as essential oils. Aromatic and medicinal plant essential oils and their components demonstrate antibacterial, antifungal, and food preservative activities against a wide range of microbial pathogens (Basim et al., 2000; Iacobellis et al., 2004; Tripathi and Kumar, 2007; Pandey et al., 2014b; Sonker et al., 2015; Gormez et al., 2016; Figure 1). These essential oils are hydrophobic liquids of aromatic compounds that are volatile and oily in nature and present in various plant parts such as twig, flower, leaf, bark, seed, and root. Many plant essential oils are useful as a flavor or aroma enhancer in cosmetics, food additives, soaps, plastics resins, and perfumes. Moreover, curiosity about essential oil applications that can act as antimicrobial agents is growing because of the broad range of activities, natural origins, and generally recognized as safe (GRAS) status of essential oils. Currently, essential oils are frequently studied for their antimicrobial (Cowan, 1999; Burt, 2004; Nedorostova et al., 2009), antifungal (Singh and Tripathi, 1999), antiulcer (Dordevic et al., 2007), antihelminthic (Inouye et al., 2001), antioxidant (Mimica-Dukic et al., 2003), anti-inflammatory (Singh et al., 1996), repellent, insecticidal, antifeedant (Isman et al., 1990; Pandey et al., 2014a), cytotoxic (Sylvestre et al., 2007), antiviral (Maurya et al., 2005), ovicidal (Pandey et al., 2011b), anesthetic (Ghelardini et al., 2001), molluscicidal (Fico et al., 2004), immunomodulatory (Mediratta et al., 2002), antinociceptive (Abdollahi et al., 2003), and larvicidal (Jantan et al., 2003) properties as well as for their use as food preservatives (Ukeh and Mordue, 2009; Pandey et al., 2014c).

FIGURE 1

Figure 1. Different activities and uses of essential oils.

Essential oils of aromatic and medicinal plants are reported to be effective against agents affecting stored products such as insects, human pathogenic fungi, and bacteria. Essential oils of Chenopodium ambrosioides, Clausena pentaphylla, Mentha arvensis, and Ocimum sanctum are contact-sensitive and act as fumigant toxicants against Callosobruchus chinensis and C. maculatus (Pandey et al., 2011a) associated with pigeon pea seeds. Similarly, the essential oil of Tanacetum nubigenum exhibit significant repellent and fumigant toxicity against Tribolium castaneum, which affects wheat during storage (Haider et al., 2015). Eucalyptus globulus essential oil has antibacterial activity against Escherichia coli and Staphylococcus aureus, thus, it is effective against both Gram-positive and Gram-negative bacteria (Bachir and Benali, 2012). In addition, other bacterial pathogens such as Haemophilus influenzae, S. aureus, S. pneumonia, and S. pyogenes were inhibited by Eucalyptus odorata essential oil under in vitro conditions (Posadzki et al., 2012). This review highlights the use of essential oils and their antifungal, fungicidal and food preservative properties in controlling fungi associated with food commodities. Additional emphasis has been given on the efficacy of essential oils against plant pathogenic bacteria as antibacterial and bactericidal.

Essential Oils and Functions of their Active Constituents

The majority of aromatic plants retain a volatile odoriferous mixture of compounds which can be extracted as an essential oil. Generally, aromatic and medicinal plants produce a wide range of secondary metabolites viz., terpenoids, alcoholic compounds (e.g., geraniol, menthol, linalool), acidic compounds (e.g., benzoic, cinnamic, myristic acids), aldehydes (e.g., citral, benzaldehyde, cinnamaldehyde, carvone camphor), ketonic bodies (e.g., thymol, eugenol), and phenols (e.g., ascaridole, anethole). Among those, terpenes (e.g., pinene, myrcene, limonene, terpinene, p-cymene), terpenoids (e.g., oxygen-containing hydrocarbons), and aromatic phenols (e.g., carvacrol, thymol, safrole, eugenol) are found to have major roles in the composition of various essential oils (Figure 2) (Koul et al., 2008). Derivatives of terpenoids and aromatic polyterpenoids are synthesized by the mevalonic acid and shikimic acid pathways, respectively (Bedi et al., 2008). Terpenoids are among an immense pool of secondary compounds produced by aromatic and medicinal plants, and they have an important role in providing resistance to pathogens. Monoterpenoids are antimicrobial in nature, result in disruptive multiplication and development of microorganisms, and interfere in physiological and biochemical processes of microorganisms (Burt, 2004). Some botanical constituents such as azadirachtin, carvone, menthol, ascaridol, methyl eugenol, toosendanin, and volkensin have reported potential to act against several bacterial and fungal pathogens as well as against insect pests (Isman, 2006; Pandey et al., 2012, 2016). Moreover, many of them have powerful bactericidal, fungicidal, and insecticidal activities and can be responsible for improved taste or toxic properties.

FIGURE 2

Figure 2. Actives compounds of essential oils. Figure as originally published in Hyldgaard et al. (2012).

Fungi such as Aspergillus flavus, Neurospora sitophila, and Penicillium digitatum are completely inhibited by Cymbopogon citratus essential oil (Shukla, 2009; Sonker et al., 2015). Essential oils from Nigella sativa, Cymbopogon citratus, and Pulicaria undulata inhibit the growth of Bacillus subtilis, Staphylococcus aureus, Pseudomonas aeruginosa and Escherichia coli (El-Kamali et al., 1998). Essential oils from Acorus, Artemisia, Chenopodium, Clausena, Curcuma, Cinnamon, Cymbopogon, Eupatorium, Foeniculum, Hyptis, Lippia, Ocimum, Putranjiva, Syzygium, and Vitex are known for their pronounced antimicrobial properties (Pandey et al., 2012, 2013b, 2014c; Sonker et al., 2015). The antibacterial properties of essential oils and their several active natural compounds against foodborne bacteria and their applications in food (Burt, 2004) could provide alternatives to conventional bactericides and fungicides (Perricone et al., 2015).

Potency of Essential Oils Against Phytopathogenic Bacteria

In cereals, pulses, fruits, and vegetables, bacterial species can cause major loss of plant quality and quantity during cultivation, transit, and storage by 20–40% of the total harvest per year. The bacterial species responsible for many diseases and loss of crops include Clavibacter michiganensis, Pseudomonas syringae pv. tomato, P. solanacearum, P. cichorii, P. syringae pv. syringae, P. putida, Erwinia carotovora, E. amylovora, E. carotovora subsp. atroceptica, E. chrysanthemi, E. herbicola, Xanthomonas citri, X. campestris, X. axanopodis pv. malvacearum, X. axanopodis pv. vesicatoria, X. axanopodis pv. campestris, X. campestris pv. raphani, X. axanopodis pv. vitians, and X. campestris pv. zinnia. Such bacteria cause substantial losses in many crops of national and international significance (Agrios, 2005). There are many essential oils that have been evaluated for their potential for antibacterial activity against these phytopathogenic bacteria under in vitro and in vivo conditions (Dorman and Deans, 2000; Iscan et al., 2003; Kotan et al., 2013). The methods used to assess the actions of essential oils against phytopathogenic bacteria include disc diffusion, agar dilution, agar well, and broth dilution (Perricone et al., 2015). Antimicrobial studies of essential oil constituents and their mode of actions more have been extensively undertaken on bacteria; however, there is limited information available about their actions on yeasts and molds.

Generally, Gram-negative bacteria are less susceptible to essential oils than Gram-positive bacteria. The outer membrane of Gram-negative bacteria contains hydrophilic lipopolysaccharides (LPS) that acts as a barrier to macromolecules and hydrophobic compounds, thus providing increased tolerance to hydrophobic antimicrobial compounds such as those found in essential oils (Nikaido, 1994, 2003; Trombetta et al., 2005). Therefore, it is difficult to predict the susceptibility of microorganisms to essential oils due to the breadth of genetic variations among species. Antibacterial activities of essential oils against a variety of phytopathogenic bacteria are summarized in Table 1.

TABLE 1

Table 1. Antibacterial investigations of essential oils against phytopathogenic bacteria.

Potency of Essential Oils Against Storage Fungi

Fungi can act as major destroyers of food commodities, including cereals, pulses, fruits, and vegetables, through the production of mycotoxins and render food unhealthy for human consumption by adversely affecting their nutritional value (Paranagama et al., 2003; Pandey et al., 2016). During storage, spoilage of stored food commodities is a chronic problem in tropical hot and humid climates. According to the FAO, foodborne fungal pathogens and their toxic metabolites can produce qualitative and quantitative losses of up to 25% of total agricultural food commodities throughout the world (Agrios, 2005). Fungal infection in food commodities results in a reduction of food quality, color, and texture as well as a reduction in nutrients present and physiological properties of food commodities (Dhingra et al., 2001). During infection, fungi can also produce mycotoxins, which can lead to famines in developing countries (Wagacha and Muthomi, 2008). With regard to molds, food contamination by Alternaria, Aspergillus, Penicillium, Fusarium, and Rhizopus spp. is of great significance because of the related health hazards and foodborne infections (Pandey and Tripathi, 2011). Hence, during storage and transit, prevention of fungal growth by essential oils could be a cost-effective approach to combat food losses. In recent years, throughout the world, the antifungal potential of essential oils is being considered significantly important (Baruah et al., 1996; Arras and Usai, 2001; Lalitha and Raveesha, 2006; Bosquez-Molina et al., 2010). The antifungal activities of essential oils are related to the associated disintegration of fungal hyphae due to the mono- and sesquiterpene compounds present in the essential oils. Moreover, essential oils amplify membrane permeability; as such compounds can dissolve in cell membranes and cause membrane swelling, thereby reducing membrane function (Dorman and Deans, 2000). Additionally, the lipophilic property of essential oils is responsible for their antifungal activity as that property gives them the ability to penetrate cell walls and affect enzymes involved in cell-wall synthesis, thus altering the morphological characteristics of the fungi (Cox et al., 2000). The present account summarizes the investigations into essential oils tested for their antifungal activity against fungi affecting food storage (Table 2).

TABLE 2

Table 2. Antifungal investigations of essential oils against fungi infecting food commodities during postharvest.

Potency of Essential Oils in Food Preservation

Research into the utility of essential oils in the preservation of food commodities in order to enhance shelf-life has been successfully carried out in recent years. Various investigators have used essential oils, either in pure or formulation forms, to enhance the shelf-life of food commodities in different storage containers such as those made of cardboard, tin, glass, polyethylene, or natural fabrics and have observed significant enhancement of shelf-life (Tripathi and Kumar, 2007; Pandey et al., 2014a). An earlier study reported that some essential oil constituents such as citral, citronella, citronellol, eugenol, farnesol, and nerol could protect chili seeds and fruits from fungal infection for up to 6 months (Tripathi et al., 1984). Essential oil from Ageratum conyzoides successfully controlled rotting of mandarins by blue mold and increased mandarin shelf-life by up to 30 days (Dixit et al., 1995). Anthony et al. (2003) investigated essential oils from Cymbopogon nardus, C. flexuosus, and Ocimum basilicum and observed that they could significantly control anthracnose in banana and increased banana shelf-life by up to 21 days. Cymbopogon flexuosus essential oil (20 μL/mL) is capable of protecting against rotting of Malus pumilo fruits for up to 3 weeks (Shahi et al., 2003). An fumigant application of essential oils from Putranjiva roxburghii was effective against A. flavus and A. niger infecting groundnuts during storage and enhanced the shelf-life of groundnut from fungal biodeterioration for up to 6 months (Tripathi and Kumar, 2007). The use of Cymbopogon pendulous essential oil as a fumigant increased groundnut shelf-life by 6–12 months (Shukla, 2009), thus proving to be more effective than P. roxburghii essential oil. These differences in efficacy of essential oils may be related to the use of oils from different plant species, as well as to their chemical composition, dose level, and storage container type.

Thyme (Thymus capitata) (0.1%) and maxican lime (Citrus aurantifolia) (0.5%) oil reduced disease incidence in papaya fruit (Bosquez-Molina et al., 2010), while cinnamon (0.3%) oil extended the storage life of banana by up to 28 days and reduced fungal disease incidence in banana (Maqbool et al., 2010). Seed dressing and fumigation of Ocimum cannum oil (1 μL/mL) enhanced the self-life of Bhuchanania (Singh et al., 2011). Clausena pentaphylla and Chenopodium ambrosioides oils, when used as fumigants in glass containers and natural fabric bags were able to protect pigeon pea seeds from A. flavus, A. niger, A. ochraceus, and A. terreus infection for up to 6 months (Pandey et al., 2013a,b). Powder-based formulations of C. pentaphylla and C. ambrosioides oils were also able to preserve pigeon pea seeds for up to 6 months (Pandey et al., 2014c). Artemisia nilagirica oil as a fumigant in cardboard improved the shelf-life of table grapes by up to 9 days (Sonker et al., 2015). Similarly, Lippia alba oil when used as an air dosage treatment in glass containers inhibited fungal proliferation and aflatoxin production in green gram (Vigna radiata) and enhanced its shelf-life by up to 6 months (Pandey et al., 2016).

Conclusion and Future Prospects

Worldwide investigations carried out on essential oils have motivated researchers to focus their interest toward the study of botanical antimicrobials. It is apparent that the use of essential oils and their derivatives has been widely described, and essential oils have been used against a wide range of pathogens. Accordingly, this review provides a brief overview of essential oils, their active constituents, and their potential as sources of antibacterials, antifungals, and food preservatives. The relevant literature summary shows that essential oils exhibit a diverse range of antimicrobial properties, and indicates their natural sustainability when used as potential biocontrol agents against fungal and bacterial pathogens. Hence, we conclude from this review that essential oils are potential sources of biocontrol products that should be further explored due to their potential to protect food commodities. Also, an essential oil-based fumigant having antimicrobial activity should have a promising GRAS status in mammalian systems. The LD₅₀ values of some botanicals like azadirachtin and carvone are found to be high in rat and are reportedly nontoxic for human consumers. Additionally, several essential oils and their constituents (e.g., carvone, carvacrol, cinnamaldehyde, thymol, linalool, citral, limonene, eugenol, limonene, and menthol) are reported by the United States Food and Drug Administration to have a GRAS status and are approved as flavor or food additives.

Essential oil applications are evolving as a means of integrating pathogens into food containers; for example, fumigants that can be useful in natural fabric and cardboard containers, and even containers made of wooden boards. Some oils can be used as light sprays and integrated as a fumigant into the commodity itself. Many essential oils and their active constituents are active against bacteria and fungi, and they can be produced from commonly available raw materials; perhaps in many cases right at the site of use so as to be rather low-cost treatments. Based on this review, it can be summarized that it is possible to develop techniques for food commodity protection without the use, or with reduced use, of commercial bactericides and fungicides. Although the available literature indicates that essential oils are host specific, biodegradable, have limited effect on non-target organisms, have low levels of mammalian toxicity. There, sustainable and commercial uses have some drawbacks, such as their cost effectiveness. Regardless, there are innumerable potential uses of essential oils and more research is needed to meet the needs of a food industry shifting toward the use of green technology.

Author Contributions

AP, PS, and NT conceived and designed the experiments. AP performed the experiments. AP and PK write the manuscript and PK and VB did the editing. All the authors read and approved the final manuscript.

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Acknowledgments

The authors (AP, PS, and NT) would like to thanks the Head, Department of Botany, DDU Gorakhpur University, Gorakhpur for providing the necessary facilities. AP is grateful to CST UP, Lucknow for financial assistance (Grant no. CST/AAS, D-09, April 3, 2007). PK thankful to Director and Head, Department of Forestry, NERIST, Nirjuli, Arunachal Pradesh, India. VB sincerely thankful to Yeungnam University, Republic of Korea.

References

Abdollahi, A., Hassani, A., Ghosta, Y., Bernousi, I., and Meshkatalsadat, M. H. (2010). Study on the potential use of essential oils for decay control and quality preservation of Tabarzeh table grapes. J. Plant Prot. Res. 50, 45–52. doi: 10.2478/v10045-010-0008-2