Essential oils as antimicrobials in food systems – A review

Accepted Manuscript Essential Oils as Antimicrobials in Food Systems– A Review Juliany Rivera Calo, Philip G. Crandall, Corliss A. O’Bryan, Steven C. Ricke PII:

S0956-7135(15)00045-6

DOI:

10.1016/j.foodcont.2014.12.040

Reference:

JFCO 4263

To appear in:

Food Control

Received Date: 9 September 2014 Revised Date:

12 December 2014

Accepted Date: 19 December 2014

Please cite this article as: Calo J.R., Crandall P.G., O’Bryan C.A. & Ricke S.C., Essential Oils as Antimicrobials in Food Systems– A Review, Food Control (2015), doi: 10.1016/j.foodcont.2014.12.040. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

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Essential Oils as Antimicrobials in Food Systems– A Review

3 4 Juliany Rivera Calo1,2 Philip G. Crandall1,2 Corliss A. O’Bryan1,2 and Steven C. Ricke1,2

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Department of Food Science, University of Arkansas, Fayetteville, AR

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Center for Food Safety, University of Arkansas, Fayetteville, AR

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*Corresponding author: Steven C. Ricke, Center for Food Safety; Department of Food Science,

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University of Arkansas, Fayetteville, AR 72704. Phone: 479-575-4678, Fax: 479-575-6936

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Email: [email protected]

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Abstract

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harmful chemicals, including many used as antimicrobials and preservatives in food.

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Consequently, interest in more natural, non-synthesized, antimicrobials as potential alternatives

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to conventional antimicrobials to extend shelf life and combat foodborne pathogens has

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heightened. Aromatic plants and their components have been examined as potential inhibitors of

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bacterial growth and most of their properties have been linked to essential oils and other

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secondary plant metabolites. Historically, essential oils from different sources have been widely

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promoted for their potential antimicrobial capabilities. In this review, mechanisms of

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antimicrobial action, and the antimicrobial properties of plant essential oils are discussed,

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including their mode of action, effectiveness, synergistic effects, major components and use in

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foods.

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Many consumers are demanding foods without what they perceive as artificial and

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Key words: natural antimicrobials; essential oils; foodborne pathogens

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1. Introduction

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effectiveness for food safety and preservation applications (Fisher & Phillips, 2008; Gyawali &

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Ibrahim, 2014; Prakash, Media, Mishra, & Dubey, 2015) and have received attention as growth

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and health promoters (Brenes & Roura, 2010). Most of their properties are due to their essential

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oils (EOs) and other secondary plant metabolite components (Brenes & Roura, 2010).

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Phytochemicals, such as EOs, are naturally occurring antimicrobials found in many plants that

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have been shown to be effective in a variety of applications by decreasing growth and survival of

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microorganisms (Callaway et al., 2011). In addition, EOs exhibit antimicrobial properties that

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may make them suitable alternatives to antibiotics (Chaves et al., 2008). These potential

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attributes and an increasing demand for natural food additive options have led to an interest in

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the use of EOs as potential alternative antimicrobials (Fisher & Phillips, 2008; Solórzano-Santos

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& Miranda-Novales, 2012).

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In recent years, aromatic plants and their extracts have been examined for their

Control of food spoilage and pathogenic bacteria is mainly achieved by chemical control,

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but the use of synthetic chemicals is limited due to undesirable aspects including carcinogenicity,

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acute toxicity, teratogenicity and slow degradation periods, which could lead to environmental

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problems, such as pollution (Faleiro, 2011). The negative public perception of industrially

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synthesized food antimicrobials has generated interest in the use of more naturally occurring

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compounds (Faleiro, 2011; Sofos, Beuchat, Davidson, & Johnson, 1998). There has been an

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extensive search for potential natural food additive candidates that retain a broad spectrum of

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antioxidant and antimicrobial activities while possessing the ability to improve the quality and

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shelf life of perishable foods (Fratianni et al., 2010). The emergence of bacterial antibiotic

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resistance and negative consumer attitudes toward food preservatives has led to an increased

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interest in the use of plant components that contain EOs and essences as alternative agents for the

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control of food spoilage and harmful pathogens (Burt, 2004; Fisher & Phillips, 2008; Nostro et

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al., 2004; Shelef, 1983; Smith-Palmer, Stewart, & Fyfe, 1998; 2001). Natural compounds with animal, plant or microbiological origins have been used in order

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to kill or at least prevent the growth of pathogenic microorganisms (Juneja et al., 2012; Li et al.,

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2011; Muthaiyan, Limayem, & Ricke, 2011; Roller & Lusengo, 1997; Tiwari et al., 2009). A

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number of naturally occurring antimicrobial agents are present in animal and plant tissues, where

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they probably evolved as part of their hosts’ defense mechanisms against microbiological

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invasion and exist as natural ingredients in foods (Sofos et al., 1998). Substances that are

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naturally occurring and directly derived from biological systems without alteration or

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modification in a laboratory setting are recognized as natural antimicrobials (Li et al., 2011;

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López-Malo, Alzamora, & Guerrero, 2000; Sirsat et al., 2009). An ideal antimicrobial would be

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one that is available in large volumes as a co-product and one that has generally recognized as

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safe (GRAS) status because it has already been part of the typical human diet for years

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(Callaway et al., 2011; Chalova et al., 2010; Friedly et al., 2009; Nannapaneni et al., 2009b).

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There is great potential for new drug discoveries based on collecting and characterizing

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traditional medicinal plants throughout the world (Dias, Urban & Roessner, 2012). In this review

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we will discuss mechanisms of antimicrobial action and the antimicrobial properties of plant

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EOs, including their mode of action, major components, effectiveness in foods, and synergistic

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or antagonistic effects for use in food systems.

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3. Essential oils

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These naturally occurring antimicrobials have extensive histories of their use in foods and can be identified from various components of the plants leaves, barks, stems, roots, flowers and

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fruits (Erasto, Bojase-Moleta, & Majinda 2004; Rahman, & Gray, 2002; Zhu, Zhang, & Lo,

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2004). Essential oils are not strictly oils, but are often poorly soluble in water as are oils.

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Essential oils often have a pleasant odor and sometimes a distinctive taste and are therefore used

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in significant amounts in the flavoring and perfume industries (Burt, 2004). Essential oils are

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usually prepared by fragrance extraction techniques such as distillation (including steam

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distillation), cold pressing, or extraction (maceration) (Burt, 2004; Edris, 2007; Faleiro, 2011;

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Kelkar, Geils, Becker, Overby, & Neary, 2006; Shannon, Milillo, Johnson, & Ricke, 2011a;

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Solórzano-Santos & Miranda Novales, 2012). Typically, EOs are highly complex mixtures of

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often hundreds of individual aroma compounds. Herbs and spices commonly used in foods have

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provided most of the EOs that have been studied for their antimicrobial activity (Cueva et al.,

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2010; Negi, 2012; Tajkarimi, Ibrahim, & Cliver, 2010). Table 1 presents a list of some common

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EOs, their sources and the most abundant chemical compounds found in the oils.

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3.1 Properties of essential oils

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The antimicrobial or other biological activities of EOs are directly correlated to the presence of their bioactive volatile components (Mahmoud & Croteau, 2002). Chemically the

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EOs consist of terpene compounds (mono-, sesqui- and diterpenes), alcohols, acids, esters,

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epoxides, aldehydes, ketones, amines and sulfides (Bakkali, Averbeck, Averbeck, & Idaomar,

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2008). The components of EOs can be divided into two groups: (i) terpene compounds and (ii)

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aroma compounds (Bakkali et al., 2008; Pichersky, Noel, & Dudareva, 2006).

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Composition of the EOs of any particular plant can be dependent on what part of the

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plant is used: flowers, green parts (leaves and stems), bark, wood, whole fruits, pericarp or seed

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only, or roots (Novak, Draxler, Gohler Franz, 2005; Olawore, Ogunwande, Ekundayo &

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Adeleke, 2005). Kuropka, Neugebauer & Glombitza (1991) demonstrated that in Achillea

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ptarmica the mono-terpenes were found in very small amounts in oils from the green parts and

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roots, while high levels were found in EOs from the flowers.

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Essential oils are thought to be produced by plants in response to stressors and therefore the conditions of growth may affect the yield and content of EOs (Theis & Lerdau, 2003). Rebey

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et al. (2012) found that a moderate water deficit (MWD) increased the number of seeds produced

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by cumin plants but a severe water deficit (SWD) decreased yield. Essential oil yield increased

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by 1.4 fold under MWD, but decreased by 37.2% under SWD in comparison. Water deficits also

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changed the profile of constituents in EOs from predominantly γ-terpinene/phenyl-1,2 ethanediol

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in the control seeds to γ-terpinene/cuminaldehyde in stressed ones.

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Badi, Yazdani, Ali, and Nazari (2004) studied the effects of plant spacing and time of harvest on the yield of EOs in thyme. Plants were harvested either at the beginning of blooming,

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full blooming or fruit set. Planting space did not significantly affect EO content, but time of

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harvest did. The maximum yield of EO and of thymol content were obtained when plants were

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placed 15 cm apart and harvested at the beginning of blooming stage.

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Many parameters affect EO yield and chemical composition of aromatic plants, such as drying methods or extraction processes (Fathi & Sefdikon, 2012). Fathi and Sefdikon (2012)

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obtained fresh leaves of Eucalyptus sargentii and used five different drying methods: sun-drying,

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shade-drying, and oven-drying (30, 40 and 50°C). Distillation methods included hydro-, water-

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and steam-distillation. Obtained oils were analyzed by capillary GC and GC-MS. Shade-dried

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samples produced the highest oil yield and 1,8-cineole content of all the drying methods used,

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while hydro-distillation produced the highest oil yield; however, the highest percentage of 1,8-

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cineole, the major constituent of Eucalyptus oil (Table 1) was obtained by water and steam

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distillation. Thus many chemical and physical factors can affect the amount and composition of

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the EOs obtained from aromatic plants. Conditions of growth and extraction can also affect the

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amounts of the major antimicrobial components of the EOs.

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3.2. Mode of action of essential oils The antimicrobial effects of EOs have been screened against a wide range of

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microorganisms over the years, but their mechanism(s) of action are still not completely

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understood. Several mechanisms have been proposed to explain the actions of the chemical

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compounds contained in the EOs (Cox et al., 2000; Burt, 2004). Essential oils are composed of

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several components and their antimicrobial activity cannot be confirmed based only on the action

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of one compound (Bajpai, Baek, & Kang, 2012). Several researchers have proposed that the

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antimicrobial action of EOs may be attributed to their ability to penetrate through bacterial

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membranes to the interior of the cell and exhibit inhibitory activity on the functional properties

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of the cell, and to their lipophilic properties (Smith-Palmer et al., 1998; Fisher & Phillips, 2009;

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Guinoiseau et al., 2010; Bajpai et al., 2012). The phenolic nature of EOs also elicits an

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antimicrobial response against foodborne pathogen bacteria (Shapira & Mimran, 2007; Bajpai et

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al., 2012). Phenolic compounds disrupt the cell membrane resulting in the inhibition of the

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functional properties of the cell, and eventually cause leakage of the internal contents of the cell

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(Bajpai et al., 2012). The mechanisms of action may relate to the ability of phenolic compounds

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to alter microbial cell permeability, damage cytoplasmic membranes, interfere with cellular

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energy (ATP) generation system, and disrupt the proton motive force (Burt, 2004; Friedly et al.,

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2009; Li et al., 2011; Bajpai et al., 2012). The disrupted permeability of the cytoplasmic

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membrane can result in cell death (Li et al., 2011).

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An important characteristic of EOs and their components is hydrophobicity, allowing the EOs to separate the lipids of the bacterial cell membrane and mitochondria and in the process

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cause the bacterial cell to become more permeable (Burt, 2004; Friedly et al., 2009). The

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interaction of EOs with microbial cell membranes results in the growth inhibition of some Gram-

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positive and Gram-negative bacteria (Calsamiglia, Busquet, Cardozo, Castillejos, & Ferret,

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2007). Gram-positive bacteria such as S. aureus, L. monocytogenes and Bacillus cereus are more

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susceptible to EOs than Gram-negative bacteria such as E. coli and S. Enteritidis

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(Chorianopoulos et al., 2004). It is generally believed that EOs mechanistically should be more

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effective against Gram-positive bacteria due to the direct interaction of the cell membrane with

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hydrophobic components of the EOs (Shelef, 1983; Smith-Palmer et al., 1998; Chao & Young,

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2000; Cimanga et al., 2002; Soković et al., 2010). Conversely, based on this premise, Gram-

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negative cells should be more resistant to plant EOs because they possess a hydrophilic cell wall

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(Kim et al., 2011). This outer layer helps to prevent the penetration of hydrophobic compounds

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(Calsamiglia et al., 2007; Ravichandran, Hettiarachchy, Ganesh, Ricke, & Singh, 2011). Deans

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& Ritchie (1987) concluded that Gram-positive and Gram-negative bacteria were equally

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sensitive to citrus EOs and their components. However, in a study by Dorman and Deans (2000)

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carvacrol and thymol acted differently against Gram-positive and Gram-negative bacteria.

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Carvacrol and thymol were able to cause disintegration of the outer membrane of Gram-negative

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bacteria, releasing lipopolysaccharides (LPS) and increasing the permeability of the cytoplasmic

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membrane to ATP (Burt, 2004).

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4. Antimicrobial effects of EOs

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Essential oils have been documented to be effective antimicrobials against several foodborne

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pathogens including Escherichia coli O157:H7, Salmonella Typhimurium, Staphylococcus

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aureus, Listeria monocytogenes, Campylobacter and others (Callaway et al., 2011). Friedman,

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Henika, & Mandrell (2002) tested 96 EOs and 23 oil compounds against C. jejuni, E. coli

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O157:H7, L. monocytogenes and Salmonella enterica and found that 27 EOs and 12 compounds

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had some activity against all 4 bacterial genera. Oils with most activity included ginger root,

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jasmine, carrot seed, celery seed, and orange bitter oils (C. jejuni); oregano, thyme, cinnamon,

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bay leaf, clove bud, lemon grass, and allspice (E. coli O157:H7); bay leaf, clove bud, oregano,

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cinnamon, allspice and thyme (L. monocytogenes); thyme, oregano, cinnamon, clove bud,

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allspice, bay leaf, and marjoram (S. enterica). Cinnamaldehyde, carvacrol, benzaldehyde, citral,

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thymol, and eugenol compounds all had some activity against all 4 organisms. Likewise Moreira,

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Ponce, de Valle, & Roura (2005) found that clove EO had the most effect on survival and growth

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of different strains of E. coli O157:H7. Soković, Glamočlija, Marin, Brkić, & van Griensven

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(2010) isolated and tested EOs from 10 herbs commonly consumed against a number of

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foodborne pathogens and spoilage organisms. They found that the greatest activity across the

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largest range of micro-organisms from EOs and components obtained from Origanum vulgare

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(oregano). The component with the greatest activity was carvacrol. All of the EOs investigated

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showed better activity against Gram-positive than Gram-negative bacteria, with the most

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resistant bacteria being the spoilage organisms Pseudomonas aeruginosa and Proteus mirabilis.

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Cherrat et al. (2014) screened EOs derived from Laurus nobilis and Myrtus communis for

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in vitro antimicrobial activity against several foodborne pathogens. The EOs inhibited the growth

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of all bacterial strains with the EO derived from L. nobilis showing the strongest activity and EO

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from M. communis showing moderate to weak activity. In general, both EOs were more active

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against Gram-positive than Gram-negative bacteria. The bacteria least resistant to both EOs were

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S. aureus, and the most resistant strains were L. monocytogenes EGD-e among the Gram-positive

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and E. coli O157:H7 among the Gram-negative strains.

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Black pepper and its component piperine have displayed antimicrobial activity against organisms found in foods including S. aureus (Sangwan et al., 2008), Salmonella (Arora and

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Kaur, 1999), B. cereus and B. subtilis (Singh et al., 2005). Karsha and Lakshmi (2010)

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determined the minimal inhibitory concentrations (MICs) of extracts of black pepper against

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Staphylococcus, Bacillus and Streptococcus were 125, 250, and 500 ppm, respectively.

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Pseudomonas was found to be more susceptible to black pepper extracts followed by

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Escherichia coli, Klebsiella, and Salmonella (62.5, 125 and 250 ppm MIC, respectively).

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Sheng and Zhu (2014) studied the effects of EOs derived from Cinnamomum cassia for antibacterial activity against the "top six" non-O157 Shiga-toxin producing E. coli (STECs) O26,

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O45, O103, O111, O121, O145. The major component of the EO was cinnamaldehyde (59.96%).

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Minimum inhibitory concentration for all tested non-O157 STECs was 0.025% (v/v), but the

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minimum bactericidal concentration was strain dependent varying from 0.05% (v/v) to 0.1%

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(v/v). Including 0.025% (v/v) of the EO in growth medium completely inhibited the growth of all

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tested non-O157 STECs for at least 24 h.

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Historically, citrus oils have been incorporated into human diets because of their flavor and beneficial health properties (Dabbah et al., 1970; Kim, Marshall, Cornell, Preston III, &

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Wei, 1995). Citrus oils are approved as generally recognized as safe (GRAS) compounds by the

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Food and Drug Administration (FDA), due to their natural role as flavoring agents in citrus

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juices (Chalova, Crandall, & Ricke, 2010; Hardin, Crandall, & Stankus, 2010; Callaway et al.,

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2011). Their use as alternatives to chemical-based antimicrobials is not a new concept as they

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have been used for medicinal purposes from ancient times into present day applications and

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considerable research has been conducted to demonstrate their bioactivity against bacteria, yeasts

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and molds (Fisher & Phillips, 2008). Approximately 400 compounds of citrus oils have been

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identified and their content depends on the specific citrus cultivar as well as the separation and

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extraction methods (Caccioni, Guizzardi, Biondi, Renda, & Ruberto 1998; Robinson, 1999; Tao

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et al., 2009). The most well-known and characterized of the EOs from citrus products include

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citrullene and limonene (Dabbah et al., 1970; Caccioni et al., 1998), which can exert potent,

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broad-spectrum antimicrobial activity (Di Pasqua, Hoskins, Betts, & Mauriello, 2006). Limonene

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has been shown to be effective against S. aureus, L. monocytogenes, Salmonella enterica and

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Saccharomyces bayanus as well as other organisms (Chikhoune, Hazzit, Kerbouche,

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Baaliouamer, & Aissat, 2013; Settanni et al., 2012). However, since limonene is a very

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hydrophobic chemical and thus is difficult to disperse in water, large concentrations must be

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used in order for limonene to be effective in foods; limonene is also susceptible to oxidative

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degradation which causes a loss of activity (Li & Chiang, 2012; Sun, 2007).

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Essential oils derived as by-products of the citrus industry have been screened for antimicrobial properties against common foodborne pathogens and several have been shown to

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possess antimicrobial properties (Dabbah, Edwards, & Moats, 1970; Callaway et al., 2008;

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Kollanoor-Johny et al., 2012; Muthaiyan et al., 2012). O’Bryan, Crandall, Chalova & Ricke

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(2008) tested 7 citrus EOs for their antibacterial act against 11 serotypes/strains of Salmonella.

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Orange terpenes, single-fold d-limonene, and orange essence terpenes all exhibited inhibitory

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activity against the Salmonella spp. on a disc diffusion assay. Orange terpenes and d-limonene

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both had MICs of 1%, while terpenes from orange essence, produced an MIC that ranged from

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0.125% to 0.5% against the 11 Salmonella tested. Nannapaneni et al. (2009a) tested seven orange

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oil fractions for their ability to inhibit the growth of Campylobacter and Arcobacter. They found

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that cold pressed terpeneless Valencia orange oil was the most inhibitory to both C. jejuni and C.

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coli, although 5-fold concentrated Valencia oil and distilled d-limonene also inhibited both

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Campylobacter spp. No inhibition of Arcobacter spp. was detected.

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Some EOs and their components have been shown to have the capacity to function as antimicrobials at low storage temperatures. Citrus EOs were investigated for their ability to

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reduce or eliminate E. coli O157:H7 or Salmonella inoculated onto beef at the chilling stage of

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processing, or during fabrication (Pittman et al., 2011b). The EOs were applied after inoculation

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by spraying at concentrations of 3% and 6% to the surface of different pieces of meat. The EOs

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significantly reduced the concentration of E. coli in comparison to inoculated-no spray or water-

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sprayed controls over a period of 90 days at refrigerated storage; total aerobic bacteria and

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psychrotrophic counts were also reduced on uninoculated briskets following treatment (Pittman

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et al., 2011b). Pendleton, Crandall, Ricke, Goodridge, & O’Bryan (2012) likewise found that

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cold pressed terpeneless Valencia oil was effective at refrigeration temperatures to reduce growth

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of several strains of E. coli O157:H7 isolated from beef.

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5. EOs in food systems

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5.1 Effect of EOs

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Factors present in complex food matrices such as fat content, proteins, water activity, pH,

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and enzymes can potentially diminish the efficacy of EOs (Burt, 2004; Firouzi, Shekarforoush,

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Nazer, Borumand, & Jooyandeh, 2007; Friedly et al., 2009). According to Vigil (2001) low pH

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can increase the solubility and stability of EOs, enhancing the antimicrobial activity. Additional

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methods to enhance EOs activity include increasing salt content, and decreasing storage

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temperatures (Burt, 2004; Friedly et al., 2009). Sivropoulou et al. (1996) reported that the

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antimicrobial effect of EOs is also concentration dependent. The production of off-flavor or

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strong odor limits the use of EOs as food preservatives to increase the safety and shelf life of

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food products (Friedly et al., 2009; Tiwari et al., 2009; Soković et al., 2010; Bajpai et al., 2012;

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Solórzano-Santos & Miranda-Novales, 2012). As a result of this, an inhibitory dose (minimum

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concentration at which no bacterial growth will be observed) instead of a bactericidal dose

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(which will kill the bacteria) is usually applied (Chorianopoulos et al., 2006, Li et al., 2011). In

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their research, Firouzi et al., (2007) reported that although in vitro work with EOs and their

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components indicated that compounds such as oregano and nutmeg possessed substantial

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antimicrobial activity, when used in food systems the amounts required were approximately 1 to

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3% higher, often higher than what would normally be organoleptically acceptable. Smith-Palmer

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et al., (1998) found that foods with higher lipid content required more EOs to inhibit bacterial

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growth. Further studies will be needed to confirm the effects of these orange EOs in vivo as well

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as incorporating them into multiple-hurdle approaches to improve food safety for meat products

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(Ricke et al., 2005; Ganesh et al., 2010; Sirsat, Muthaiyan, & Ricke, 2011).

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Friedman et al. (2004) evaluated several EOs for antibacterial activity against the E. coli

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O157:H7 and S. Hadar in apple juice. Compounds most active against E. coli included

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carvacrol, oregano oil, geraniol, eugenol, cinnamon leaf oil, citral, clove bud oil, lemongrass oil,

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cinnamon bark oil, and lemon oil. The most active compounds against S. Hadar were Melissa oil,

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carvacrol, oregano oil, terpeineol, geraniol, lemon oil, citral, lemongrass oil, cinnamon leaf oil,

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and linalool. Activity increased with incubation temperature and storage time, and was not

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affected by acidity. Eugenol, menthol, and thymol have also been successfully tested as a coating

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for strawberries to delay post-harvest decay (Wang, Wang, Yin, Parry & Yu, 2007). Lu, Joerger

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and Wu (2014) developed a wash solution containing thymol that achieved a 7.5 log reductions

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of Salmonella on grape tomatoes as compared to the control, without negatively impacting the

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color, pH, texture, or sensory quality of the tomatoes during 16-day storage at 4 and 22o C. The

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treatment also achieved a 1.3 log reduction of total aerobic bacteria on the tomatoes and a 5 log

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reduction of Salmonella in spent wash water.

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In addition to fruits and vegetables, EOs antimicrobial activities have also been evaluated in meat products. Tunisian sage (Salvia officinalis L.) and Peruvian peppertree (Schinus molle

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L.) EOs were added into minced beef meat inoculated with S. Anatum and S. Enteritidis and the

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beef was stored under refrigeration for up to 15 days. Only bacteriostatic effects were observed

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for concentrations of less than 0.1% (w/v), but at concentrations of up to 3.0%, bactericidal

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effects were apparent, and more pronounced with increasing concentration (Hayouni et al.,

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2008). Naturally occurring C. jejuni isolated from a whole retail chicken was used to determine

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antimicrobial capacities of the cold pressed terpeneless Valencia orange oil and limonene when

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applied on chicken legs and thighs (Nannapaneni et al., 2009a). The two types of chicken parts

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did not influence the antimicrobial strength of either orange fraction; C. jejuni cells attached to

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the skin were resuced approximately 1.5 to 2 log compared to the control, and limonene caused

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complete inhibition without recovery of detectable viable cells.

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Bukvicki et al. (2014) evaluated the effects of Satureja horvatii in a ground pork product. The main components of the oil were p-cymene (33.1%), thymol (26.1%) and thymol methyl

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ether (15.1%). The EO inhibited growth of L. monocytogenes inoculated into the meat. The color

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and flavor of uninoculated meat treated with the EO improved during 4 days of refrigerated

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storage.

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da Silveira et al. (2014) evaluated the antimicrobial activity of bay leaf EO in fresh

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Tuscan sausage stored at 7°C for 14 d. Sausages were treated at 0.05 g/100 g or 0.1 g/100 g and

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their shelf life was compared to a non-treated control. The EO was able to reduce the population

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of total coliforms by nearly 3 log CFU/g and to extend the product shelf life for two days.

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Consumers found the sensory characteristics of the treated sausages to be acceptable at both

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concentrations.

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5.3 Encapsulation, films and vapors Nano- or microencapsulation of EOs could offer possible solutions to solve challenges

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facing their applications in food. Pan et al. (2014) studied thymol encapsulated in sodium

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caseinate and found that the encapsulated thymol was more effective than un-encapsulated

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thymol in inhibiting foodborne pathogens in milk, due to the enhanced distribution and solubility

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of the encapsulated EO. Chen, Zhang and Zhong (2015) co-encapsulated eugenol and thymol in

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zein/casein nanoparticles which were subsequently spray dried. The spray dried complexes

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rehydrated easily and produced a stable dispersion. The encapsulated EOs showed controlled

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release in 24 h, with the encapsulated eugenol showing a higher release rate than thymol.

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Bactericidal and bacteriostatic effects were observed in milk whey for E. coli O157:H7 and L.

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monocytogenes Scott A, respectively.

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Kafirin is a protein extracted from sorghum which is widely used in food coatings and

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films (Taylor, Taylor, Dutton, & de Kock, 2005). Giteru et al. (2015) developed a kafirin film

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containing citral and quercetin as natural antimicrobial and antioxidant agents. They determined

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that films incorporated with citral had strong antimicrobial activity against C. jejuni, L.

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monocytogenes and P. fluorescens. However, both EOs imparted a yellowish color to films, and

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significantly lowered the film oxygen permeability, tensile and rate of water vapor transmission.

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Peretto et al. (2014) prepared edible films of strawberry puree with carvacrol and methyl

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cinnamate and used them in clamshells to provide controlled release of vapors without direct

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contact with the fruit. Fresh strawberries were packed in the clamshells and kept at 10oC for 10

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days with 90% relative humidity. They observed a significant delay and reduction in the severity

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of visible decay in fruit that was packed in the clamshells with the treated films and berries

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remained firmer and brighter in color as compared to untreated strawberries.

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Mushrooms are a fresh product that are subject to rapid deterioration due to their delicate nature as well as high respiration rate which contributes to enzymatic browning. Active

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packaging using EOs could be one solution to this problem. Gao, Feng and Jiang (2014)

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fumigated button mushrooms with EOs including clove, cinnamaldehyde, and thyme and

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determined effects on browning and postharvest quality during 16 days of cold storage. Results

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indicated that all EOs could inhibit the senescence of mushrooms, although the most effective

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compound was cinnamaldehyde. Echegoyen and Nerin (2015) determined the effect of active

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packaging with cinnamon oil on postharvest deterioration in mushrooms. They found that the

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active packaging prevented weight loss and browning when compared to non-active paraffin-

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based packaging. They also found better results when the bottom and walls of the trays were

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covered as compared to the bottom alone.

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5.2 Combined effects

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The use of antimicrobials in combination is also referred to as multiple-hurdle technology

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(Leistner & Gorris, 1995; Ricke, Kundinger, Miller, & Keeton, 2005; Friedly et al., 2009; Sirsat,

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Muthaiyan, & Ricke, 2009). The antibacterial effects of organic acids increase as the

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concentration increases (Dickson & Anderson, 1992). Organic acids, chlorine dioxide, and

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trisodium phosphate are classified as safe (GRAS) and effective sanitizers (Cutter, 2000).

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Besides being used as food additives and preservatives, organic acids and their salts also have

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food processing applications (Ricke, 2003a; Ricke et al., 2005; Milillo, Martin, Muthaiyan, &

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Ricke, 2011). Organic acids have several different antimicrobial mechanisms, such as disruption

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of intracellular pH, osmotic stress, and membrane perturbation (Russell, 1992; Hirshfield,

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Terzulli, & O’Byrne, 2003; Ricke, 2003a). Friedly et al., (2009) observed significant synergistic

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antimicrobial properties against Listeria by combining citrus EOs with four different organic

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acids, citric, malic, ascorbic and tartaric acid, making citrus EOs a more attractive antimicrobial

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control measure. Their study revealed that low concentrations of citrus EOs in combination with

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organic acids could be effective to control Gram-positive microbial growth, in this case Listeria.

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By combining organic acids and EOs against Listeria, Friedly et al., (2009) concluded that their

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findings would allow for a reduction of the concentration of EOs by more than 10-fold. Zhou et

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al., (2007) reported that the combination of thymol or carvacrol with EDTA, acetic acid, or citric

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acid all resulted in significantly reduced populations of S. Typhimurium. In samples treated with

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combinations, these antimicrobials exhibited synergistic effects compared with samples treated

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with thymol, carvacrol, EDTA, acetic acid, or citric acid alone (Zhou et al., 2007). Shannon et al.

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(2011b) evaluated the effectiveness of nisin and cold-pressed terpeneless Valencia oil (CPTVO)

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on limiting L. monocytogenes growth. A combination of 0.025% CPTVO and 26 IU/mL nisin,

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did not inhibit growth relative to the control, but when CPTVO was added at 0 h followed by the

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introduction of nisin at 15 h there was a statistically significant reduction in growth.

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Many EOs also show synergistic antimicrobial activity when used in combination. For

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example, the minimum bactericidal concentration (MBC) of carvacrol, thymol, and eugenol

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against Listeria innocua was 150, 250, and 450 mg/kg, respectively (García-García, López-Malo

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& Palou, 2011). Mixtures of 62.5 mg/kg of thymol and 75 mg/kg of carvacrol, or 56.25 mg/kg

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thymol and 125 mg/kg eugenol completely inhibited growth of L. innocua as did a combination

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carvacrol-thymol-eugenol of 75, 31.25, and 56.25 mg/kg. Therefore, combinations of EOs could

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reduce the amount needed as antimicrobial preservatives to lower the cost and potential impacts

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on sensory quality.

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Thanissery and Smith (2014) found that a combination of thyme and orange EOs (TOC)

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inhibited the growth of both Salmonella and Campylobacter when used at a level of 0.5%. They

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then evaluated the effect of a salt-phosphate marinade solution with 0.5% TOC applied by

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vacuum tumbling on the shelf life of broiler breast fillets (skinless) and whole wings. The total

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aerobic count on fillets was significantly reduced as compared to the control, although not on the

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wings, indicating that a higher level would be necessary for skin on products.

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Thymol is able to disintegrate the outer membrane of bacteria and increase the

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permeability of the cytoplasmic membrane (Lambert et al. 2001; Burt 2004; Xu et al. 2008).

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Ilhak and Guran (2014) combined thymol with sodium lactate to test whether the thymol would

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facilitate the diffusion of the sodium lactate into bacterial cells of L. monocytogenes and S.

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Typhimurium in a processed food, fish patties stored at refrigeration for 5 days. The combination

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of thymol and sodium lactate did not show a significant inhibition on the L. monocytogenes when

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compared to sodium lactate alone, but thymol and sodium lactate did show a synergistic effect on

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S. Typhimurium during the storage period. Thymol was used in these studies at only 0.1%

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because in preliminary studies the researchers had found that 0.25% thymol was unacceptable to

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consumers. They concluded that lower levels of thymol would be suitable for use in processed

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foods containing many spices to mask the flavor of the thymol.

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Cherrat et al. (2014) combined traditional heat, pulsed electric field treatments (PEF) or

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high hydrostatic pressure (HHP) treatments with a very low dose (0.2 µL/mL) of L. nobilis or M.

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communis EOs. All combinations showed synergistic lethal effects against E. coli O157:H7 and

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L. monocytogenes EGD-e at both pH 7.0 and 4.0, in some cases allowing up to 5 log inactivation

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of bacteria.

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de Oliveira et al. (2015) determined the effect of a combination of carvacrol and 1,8cineole against a mixed culture of L. monocytogenes, Aeromonas hydrophila and P. fluorescens

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in minimally processed vegetables. Carvacrol had an MIC of 1.25 and 1,8 cineole of 40 mu

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L/mL, while the Fractional Inhibitory Concentration (FIC) index of the combined compounds

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was 0.25 against the mixed inoculum, suggesting a synergic interaction. Use of the compounds

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alone or in combination in vegetable-based broth or inoculated fresh vegetables caused a

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decrease in viable cell counts over 24 h.

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7. Conclusions

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In summary, many EOs exhibit activity against foodborne pathogens and spoilage

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organisms in vitro, and to a smaller degree, in foods. Gram-positive organisms seem to be much

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more susceptible to EOs than Gram-negative organisms. Future research should focus on the

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effectiveness of different EOs in various food matrices. Synergism between EOs and other

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compounds or with other processing techniques will also need to be investigated before they can

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be applied commercially.

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Ilhak, O. I., & Guran, H. S. (2014). Combined antimicrobial effect of thymol and sodium lactate against Listeria monocytogenes and Salmonella Typhimurium in fish patty. Journal of Food Safety, 34, 211-217.

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Table 1. Main constituents of select essential oils derived from plants

% 59.2

Piper nigrum

linalyl acetate linalool piperine

16.8 9.5 33.5

Carrot (juice)

Daucus carrot L.

Cinnamon (bark)

Cinnamomum verum

Syzygium aromaticum

Coriander (seeds)

Coriandrum sativum

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Clove (buds)

Nigella sativa L.

Eucalyptus oil

Eucalyptus spp

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Cumin (seeds)

Fennel (seed)

Key lime

Lemongrass

piperolein Piper amide carotol sabinene beta-caryophyllene alpha-pinene transcinnemaldehyde limonene Eugenol Eugenol eucalyptol ∆3-Carene

Foeniculum vulgare L.

Citrus aurantifolia (Christm.) Swingle

Cymbopogon citratus (DC) Stapf.

Reference Nabiha, Abdelfatteh, Faten, Hervé & Moncef, 2010

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Main components limonene

Singh, Marimuthu, Murali, & Bawa, 2005

SC

Black pepper (berry)

Latin name Citrus bergamia

20.2 12.8 8.0 6.1 68.4

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Plant source Bergamot (peel)

13.2 4.4 7.5 3.2 60.5

Ma et al., 2015

Baratta et al., 1998

Naveed et al., 2013 Teixeira et al., 2013

Trans-Anethol

18.2 6.5 37.6 31.4 5.6 4.570.4 0.020.9 1.017.6 56.4

Fenchone Methyl chavicol Limonene

8.3 5.2 53.8

Costa et al., 2014

γ-terinene Β-pinene Geranial

16.5 12.6 45.7

Baratta et al., 1998

γ-terpinene camphor Thymoquinone p-cymene α-thujene 1,8-cineole cryptone α-pinene

Singh et al., 2014

Elaissi et al., 2012

Roby, Sarhan, Selim, & Khalel, 2013

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Rosmarinus offcinalis L.

20.8

Baratta et al., 1998

γ-terpinene α-Terpinene 1,8-Cineole

14.1 9.2 46.6

Baratta et al., 1998

α-pinene limonene

11.8 9.3

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Rosemary

Marjorana hortensis Moench

3.9 2.7

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Marjoram

myrcene 6-Methylhept-5en-2-one Terpinen-4-ol