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Food Research International 45 (2012) 722–734

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Review

Control of Salmonella in foods by using essential oils: A review

Vivek K. Bajpai a, Kwang-Hyun Baek a, Sun Chul Kang b,⁎a School of Biotechnology, Yeungnam University, Gyeongsan, Gyeongbuk 712-749, Republic of Koreab Department of Biotechnology, Daegu University, Gyeongsan, Gyeongbuk 712-714, Republic of Korea

⁎ Corresponding author. Fax: +82 53 850 6559.E-mail address: [email protected] (S.C. Kang).

0963-9969/$ – see front matter © 2011 Elsevier Ltd. Alldoi:10.1016/j.foodres.2011.04.052

a b s t r a c t
a r t i c l e i n f o
Keywords:
SalmonellaFood poisoningPlant-based antimicrobialsPEOsAntibiotic resistance
During the past several years, limit of Salmonella infections has been exceeded dramatically. In spite ofachieving a low rate infection in Salmonella infections, this microbe has become a challenge in food industrydue to its wide-spread distribution worldwide. Salmonella bacteria are not only responsible for mild to severeinfections but also they cause life-threatening infections. Salmonella bacteria are zoonotic in nature and ham-per the food quality severely as well as being hazardous to human society. Several types of serotypic Salmo-nella have been reported; however, very less numbers of pathogens are infection responsible. Increase infoodborne infections caused by Salmonella types mainly occurs due to the development of new specific fea-tures in Salmonella majority, making them to adapt in any environmental condition. Also the alterations inhuman society with recent food processing and marketing methodology with live breeders contribute to fa-cilitate these outbreaks. Salmonella resistant to commercial antibiotic drugs has emerged as a great healthconcern to the consumers. Literature survey has revealed that infection with Salmonella resistant to antibi-otics has played a vital role to increased rate in foodborne infectious diseases. Extensive use of antibioticsin food industry against foodborne pathogens or food models has resulted in additional antibiotic resistanceto Salmonella which has become a matter of great concern to the public health. There has been an increasingconcern worldwide on therapeutic values of natural products. Nature has presented to humanity the gift ofvast therapeutic antimicrobial agents of plant origins. There are multitudes of potential useful bioactive sub-stances to be derived from plants. The significance of drugs cannot be over-emphasized with the recent trendof high percentage of resistance of microorganisms to the present day antibiotics. This review provides theinformative literature data on antibacterial efficacy of plant essential oils (PEOs) and their volatiles. In addi-tion, the suitability of PEOs and their volatile components for their practical applications in food or food prod-ucts against Salmonella, a common cause of salmonellosis food poisoning has also been focused. The currentknowledge of volatile oils and contents in food model system to control Salmonella has been discussed. Also abrief description on the legal aspects on how to use the volatile oils in food system has been presented, andthe area for future research has been proposed. A mode of antibacterial action of PEOs along with their chem-ical nature has also been described. Although some data on Salmonella-related issues are presented, this re-view chiefly focused on in vivo practical utilization of plant volatile oils and components in food model-system as natural anti-Salmonella agents.

© 2011 Elsevier Ltd. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7232. Control of Salmonella by the plant-based natural antimicrobials . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 723

2.1. PEOs: an overview . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7232.2. Chemistry of PEOs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7242.3. Mechanism of action of PEOs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7252.4. Antibacterial efficacy of PEOs in food model system . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7252.5. Salmonella control in meat and poultry products . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7272.6. Salmonella control in milk and dairy products . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7272.7. Salmonella control in fruits, vegetables and juices . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 728

3. Applications of PEOs in food packaging. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7284. Application of PEOs or their components in poultry . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 728

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723V.K. Bajpai et al. / Food Research International 45 (2012) 722–734

5. Synergism and antagonism between oil components . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7306. Laws and regulations on the use of PEOs in foods. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7307. Future perspectives . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7308. Conclusion. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 731Acknowledgments. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 731References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 726731

1. Introduction

Salmonella bacteria have become the major cause of foodbornediseases which has raised a great safety concern to public health. Inseveral geographic regions, a large proportion of foodborne diseasesare confirmed by the hazardous salmonellosis caused by infectiousSalmonella (Rabsch, Tschäpe, Andreas, & Bäumler, 2001). Salmonellafood poisoning can affect any person, especially with weakened im-mune systems (El-Gazzar & Marth, 1992). In these persons, the infec-tion may initiate and spread dramatically to various body sites if theperson is not treated with suitable antibiotics. In the present time, in-tensive cases of foodborne diseases caused by Salmonella have dra-matically surplused (Humphrey & Jorgensen, 2006). The meatproducts contaminated with Salmonella bacteria have become an im-portant issue which has enhanced the number of cases of foodbornediseases (Humphrey & Jorgensen, 2006). It has been reported thatmeat products infected with Salmonella bacteria were found to playa necessary role to increase the incidences of foodborne outbreaks,hence were not subjected to distribute in the marketable form(EFSA, 2009).

Food industry, although having a number of food preservatives, isexperiencing a lack of potent food preservative agents to secure thesafety of food or food products (Mead et al., 1999). Although, antimi-crobial drugs have supported to control the foodborne pathogens ordiseases in food systems, however, acquired resistance to these anti-microbial agents is a major drawback due to their exerting severalside effects (O'Brien, 2002). Hence, certain effective antimicrobialdrugs are needed for their practical applications to control foodbornepathogens.

The plant volatiles or plant essential oils (PEOs) are plant secondarymetabolites which are biosynthesized in glandular structures of a plantcell. PEOs are known to work as potential antimicrobial agents havingthe ability to control foodborne pathogenic bacteria (Bajpai, Rahman, &Kang, 2008; Burt, 2004; Oussalah, Caillet, Sauciere, & Lacroix, 2007).Use of PEOs in food and beverage industries has been exploited for de-cades. Besides, they have been shown to work as potent antibacterialagents because of the presence of bioactive volatile components(Conner, 1993; Oussalah et al., 2007). Chemistry of PEOs was found tosupport the phenomena that these oils containing volatile componentswere shown to serve as the most potent antimicrobials (Botsoglou,Govaris, Botsoglou, Grigoropoulou, & Papageorgiou, 2003; Exarchou etal., 2002). Themajor drawback of food products is that they are easily de-teriorated by foodborne pathogens during their processing (Gould,1996) which has urgently requested to search for new and effectivefood preservatives (Davidson, 1997). In previous time, due to the lackof effective antimicrobials and literature unavailability (Board & Gould,1991), improved food preservation techniques have promoted thesearch for new antimicrobial preservatives in food industry. It has beenreported that various factors are responsible for the biological efficacyof PEOs to serve as potent antibacterial agents in food system which in-clude temperature, appearance, pH, load of microbial flora and favorableenvironment (Skandamis, Tsigarida, & Nychas, 2000). Also, some of thePEOs for their practical utilization serve as potent food preservatives inmeat production than commercial antimicrobials (Tassou, Drosinos, &Nychas, 1995). Several PEOs have effectively controlled the load of mi-crobial pathogens in various food products practically (Barbosa et al.,

2009; Skandamis & Nychas, 2001; Tsigarida, Skandamis, & Nychas,2000). Hence, addition of PEOs and their volatile components can beused against pathogenic bacteria of Salmonella species which will serveas green preservatives to food industry (Conner, 1993; Dorman &Deans, 2000). Previously the researches on PEOs have been performedextensively to support their biological efficiency (Burt & Reinders,2003; Cox et al., 2000; Delaquis, Stanich, Girard, & Mazza, 2002;Mejlholm & Dalgaard, 2002). Moreover, the PEOs and their volatileshave been shown to possess the activity against various pathogenic bac-teria (Helander et al., 1998; Kim, Marshall, & Wei, 1995a).

In general, the biological efficacy of PEOs is confirmed due to theirchemical components that include phenolics or the components fromterpene origin (Conner, 1993; Didry, Dubreuil, & Pinkas, 1993). Al-though, all the PEOs have been shown to exert antimicrobial efficacy,a number of variations have been reported in their chemical natureand the amount of their volatiles reason being variations in the collec-tion time of sample, abundance and/or lack of mineral components,distribution, changes in genetic levels, environmental conditions andthe portion of the plant used for distillation (Salgueiro et al., 1997;Venskutonis, 1996). Although, several PEOs, as a whole, show potentbiological efficacy (Kim et al., 1995a; Lambert, Skandamis, Coote, &Nychas, 2001), the antimicrobial efficacy of PEOs has been creditedto the components present in higher amount. Besides, the compo-nents present in lower amount have been shown to exert synergisticeffect with the major components of the oil (Paster, Menasherov,Ravid, & Juven, 1995).

Several concerns have been raised to minimize the load of chemicalpreservatives in foods or storage food products. Recently, the use ofPEOs has become a focal area of research for their practical applicationsto control the hazardous pathogens in food model system (Marino,Bersani, & Comi, 2001). Pathogenic microbes in storage food or foodproducts are responsible to degrade or deteriorate the quality of foodproducts, resulting in the emerging foodborne diseases in various re-gions of the world (Mead et al., 1999). In this regard, applications ofPEOs, being potent antimicrobials and low toxic in nature, can be agood strategy to control or inhibit the foodborne pathogenic bacteriain marketable food products or processed foodswith higher percentageof consumer acceptability (Deans & Sbodova, 1990; Paranagama,Abeysekera, Abeywickrama, & Nugaliyadd, 2003).

2. Control of Salmonella by the plant-based natural antimicrobials

2.1. PEOs: an overview

Although food industry has been enriched with several food prac-tices, consumers are still aware about the health problems caused byfoodborne pathogenic bacteria (Burt, 2004; WHO, 2002a). A largeproportion of population is suffering from the diseases caused byfoodborne pathogenic bacteria in several geographical regions of theworld (Burt, 2004; WHO, 2002a). This has requested an urgent needto develop new and effective natural antimicrobials to combat withthe diseases caused by foodborne pathogenic bacteria (Burt, 2004;Leistner, 1978). As per Burt (2004), Western society has appearedto experience the concern that corporates the chemical preservativeswith a lesser amount of environmental impact (Smid & Gorris, 1999;Tuley de Silva, 1996). Even though small amount of salt intake can

724 V.K. Bajpai et al. / Food Research International 45 (2012) 722–734

lower the possibilities of heart-related diseases, certain additionalsupplements are required to retain the shelf-life of food products(Burt, 2004; WHO, 2002b). Hence, there might be a high demand ofalternative strategies to prolong the shelf-life of processed or cookedfoods using PEOs (Burt, 2004).

Naturally PEOs, having aroma and flavor are isolated from the vari-ous parts of the plants (Burt, 2004; Guenther, 1948). The PEOs for com-mercial utilization can be isolated using various methodologies whichinclude steam distillation, solvent extraction, and expression (Burt,2004; Van de Braak & Leijten, 1999). According to Burt (2004), aboutthree thousand PEOs having potent biological efficacy are commercial-ized, and having significant contribution to aroma and flavor industries(Van de Braak & Leijten, 1999). As reported previously, most of the PEOsexert potent biological efficacy (Boyle, 1955; Burt, 2004; Carson & Riley,1995; Deans & Ritchie, 1987; Guenther, 1948; Mourey & Canillac, 2002;Shelef, 1983). The antimicrobial or other biological activities of PEOs aredirectly correlated to the presence of their bioactive volatile compo-nents (Guenther, 1948; Mahmoud & Croteau, 2002).

According to Burt (2004), the antibacterial activity of PEO wasreported to perform first time in 1881 (Boyle, 1955). Further, in laterdates, the use of PEOs was exploited in other industries; however, theextreme utilization rate of PEOs was reported to have in aroma and fla-vor industries (Burt, 2004; Guenther, 1948). Industrial utilization ofPEOs has been performed greatly at wide range of utilization includingvarious industries (Bauer & Garbe, 1985; Burt, 2004; Van de Braak &Leijten, 1999; Van Welie, 1997). Also the role of PEO components orthose prepared synthetically has been exploited vigorously in severalbeneficial industries to secure the food safety (Oosterhaven, Poolman,& Smid, 1995). A list of selected antimicrobial PEO components hasbeen given in Fig. 1. The role of PEOs and PEO volatiles as an alternativeto animal foods has been reported previously (Burt, 2004; Ilsley, Miller,Greathead, & Kamel, 2002; Van Krimpen&Binnendijk, 2001). Combina-tions of various PEOs with natural and herbal forms are also available inthe market for their practical utilization (Burt, 2004; Cutter, 2000;Mendoza-Yepes, Sanchez-Hidalgo, Maertens, & Marin-Iniesta, 1997).

Extension of prolonged-life of food is needed from the contamina-tion caused by foodborne pathogenic bacteria. Old food preservativepractices cannot control the food contamination, hence, other new

Cinnamaldehyde CarvacrolGeraniol

Thymol

Spathulenol-cadinol

(+)-carvone

-pinene

-farnesene

Humulene

-caryophylleneBornylen

Glob

Perillaldehyde

Fig. 1. Selected antimicrob

methodologies are required to maintain the shelf-life of food productswhich include solid and vapor phase techniques (Lopez, Sanchez,Battle, & Nerin, 2005). Besides, concerns on reducing chemical preser-vatives in food industry have been raised due to the adversary effectsof chemical preservatives, resulting in the release of toxic materialsinside the packed food products. Use of PEOs can be an effective appli-cation as food preservatives naturally due to their potent antimicrobi-al nature. PEOs have been thoroughly screened for their potentialsusing various test assays. Following these assays, the PEOs directlycome in the contact of test organism, and the inhibitory effect is de-fined directly or by measuring the physical properties (Angioni etal., 2004; Benkeblia, 2004; Burt, 2004; Holley & Patel, 2005; Lopezet al., 2005).

Evolution methodologies for determining the antibacterial efficacyof PEOs include diffusion assay. In this assay, antibacterial activity ismeasured as an inhibitory zone around the disk impregnated withPEO (Dadalioglu & Evrendilek, 2004; Kim et al., 1995a; Sridhar,Rajagopal, Rajavel, Masilamani, & Narsimhan, 2003). Another focalarea of application of PEOs is direct contact assay, in which the PEOsare added to the packed food stuff (Caccioni, Guizzardi, Biondi,Renda, & Ruberto, 1998). Besides, new insights can be measured bycorrelating the antimicrobial environment of PEO inside the packag-ing with its known antimicrobial potential (Batlle, Colmsjo, &Nilsson, 2001; Chen & Pawliszyn, 2003; Lopez et al., 2005).

Various antimicrobial vapor assay protocols have been evaluatedfor determining the antimicrobial efficacy of several PEOs (Lopez etal., 2005). Although, variations in the antimicrobial activities ofPEOs have been observed, the less sensitivity of negatively chargedbacteria is attributed to the extra polysaccharide layer as comparedto positively charged bacteria lacking this outer cell wall coverage.

2.2. Chemistry of PEOs

PEOs are the low molecular weight volatile mixtures, biosynthe-sized in various organs of plants. The chemical nature of PEOs belongsto the composition of terpene compounds (mono-, sesqui- and di-terpenes), which are mainly obtained as hydrocarbon compounds orthe derivatives of oxygen molecule. A few components of PEOs are

-thujene-myrcene

trans-dihydrocarvone-cadinene

Eugenol

Valerianol

2-phenyl-2-butene

2- -pinene

Linalool

ulol

Eucalyptol

Farnesol

ial principles of PEOs.


nitrogenous or sulfur in nature which are found as alcohols, acids,esters, epoxides, aldehydes, ketones, amines and sulfides (Bakkali,Averbeck, Averbeck, & Idaomar, 2008). The components of PEOsare divided in two groups: (i) compounds from terpene origin and(ii) aroma compounds (Bakkali et al., 2008; Pichersky, Noel, &Dudareva, 2006).

Terpene compounds have natural occurrence in plants found asmajor components of most of the PEOs. Based on their structuraland functional properties, terpene compounds have been classifiedaccording to their basic structural unit isoprene containing five car-bons (Bakkali et al., 2008). In the formation of terpenes, prenyldipho-sphate serves as a precursor (Bakkali et al., 2008). The terpenecompounds exist in the form of mono-, sesqui-, hemi-, di-, tri- andtetraterpenes. The monoterpenes containing two isoprene units areresponsible to construct the major portion of all the PEOs. These com-pounds work as carbure, alcohol, aldehyde, ketone, ester, ether, per-oxide and phenols (Bakkali et al., 2008). The sesquiterpenecompounds contain three isoprene units and the functional proper-ties are very close to monoterpene compounds.

The aromatic compounds are the derivatives of phenylpropane(Bakkali et al., 2008), which are aldehydes, alcohols, phenols, meth-oxy and methylene dioxy in nature. A few nitrogen and sulfur com-pounds present in PEOs are also characterized as plant essentialconstituents (Bakkali et al., 2008).

2.3. Mechanism of action of PEOs

Previously several researches have been performed on PEOs inorder to confirm their biological efficacy against bacteria and fungi,however, no trust worthy data have been obtained on the mode of ac-tion of PEOs so far (Lambert et al., 2001; Nychas, 1995; Shelef, 1983).Because the PEOs contain a number of components, hence the antimi-crobial action cannot be confirmed by the action of a single com-pound. Besides, different PEOs or their different components showantimicrobial mode of action not only at a particular location butalso at different cell sites (Carson, Mee, & Riley, 2002; Skandamis &Nychas, 2001). Hydrophobic nature of PEOs makes them to interactwell with lipid membrane of bacterial pathogens, resulting in theleakage of the inner cell components of the cell as well as affectingpotassium ion reflux, and eventually leading to cell death (Cox etal., 2000; Denyer & Hugo, 1991; Gustafson et al., 1998; Helander etal., 1998; Knobloch, Weigand, Weis, Schwarm, & Vigenschow, 1986;Lambert et al., 2001; Sikkema, De Bont, & Poolman, 1995). Generally,phenolic nature of PEOs makes them to work effectively against food-borne pathogenic bacteria (Farag, Daw, Hewedi, & El-Baroty, 1989;Juliano, Mattana, & Usai, 2000; Lambert et al., 2001). The phenoliccompounds disrupt the cell membrane as well as affectively inhibitthe functional properties of the cell, and eventually leaking theinner materials of the cell (Rasooli, Rezaei, & Allameh, 2006;Sikkema et al., 1995). Besides, chemistry of the composition of PEOsor their volatile compounds have great impact on their antimicrobialmechanism, phenolics containing OH− group, hence, work out effec-tively against foodborne pathogenic bacteria (Dorman & Deans, 2000;Ultee, Slump, Steging, & Smid, 2000).

Volatiles from PEOs not only work on single target site in the cellbut also they bind to protein structures of the cell. Bacterial cell mem-brane contains the enzymatic proteins to maintain the functionalproperties, and storage of hydrocarbons to lipid membrane canmake the changes in the building block of lipids and proteins, result-ing in the permeability of the cell components (Juven, Kanner,Schved, & Weisslowicz, 1994; Knobloch, Pauli, Iberl, Weigand, &Weis, 1989; Sikkema et al., 1995). Some of the PEOs and their vola-tiles are found to be responsible in inhibiting the enzymatic proteinsin some bacterial pathogens (Wendakoon & Sakaguchi, 1995).

In addition to this, terpene compounds have beenwell known to af-fect on the bacterial cell membrane, thereby resulting in the changes of

cell functions, leakage of cell components as well as making starvingconditions to survive the cell or cell components (Fisher & Phillips,2008). Hence, the functions of cell components including nucleus canbe reduced by the effect of PEOs or their volatiles due to the permeabil-ity changes that occurred in the membrane of bacterial cell (Fisher &Phillips, 2008; Oussalah, Caillet, & Lacroix, 2006). The effect of the per-meability on the membrane of bacterial cell also results in the releaseof the ionic molecules from the cell (Fisher & Phillips, 2008; Raybaudi-Massilia, Mosqueda-Melgar, & Martín-Belloso, 2006).

2.4. Antibacterial efficacy of PEOs in food model system

A very less amount of research was conducted on commercialPEOs as natural food preservatives up to the year 1990 (Board &Gould, 1991; Burt, 2004). After that, several researches were per-formed on PEOs to confirm their efficacy as natural food preserva-tives. Although, it is now well known that higher amount of PEOsused in vitro assays is also essential to confirm their in vivo efficacywhile using in food models, contradictory results have also been ob-served in few cases (Karatzas, Kets, Smid, & Bennik, 2001;Mendoza-Yepes et al., 1997; Pandit & Shelef, 1994; Shelef, 1983;Smid & Gorris, 1999; Stecchini, Sarais, & Giavedoni, 1993; Ultee &Smid, 2001; Wan, Wilcock, & Coventry, 1998).

In a study conducted on salad by inoculating a foodborne patho-gen reported that the PEO of oregano could suppress the growthof Salmonella community in a very less time (Koutsoumanis,Lambropoulou, & Nychas, 1999) for which the intrinsic and extrinsicproperties used were the causative factors to decline the growth ofthis foodborne pathogen. Time-based declining pattern of Salmonellawas also evaluated in order to compare the efficacy of PEOs using twofood models (Gibson, Bratchell, & Roberts, 1988). The food modelsused by Gibson et al. (1988) were found suitable to define the useful-ness of oregano oil for confirming the bacterial population under sev-eral intrinsic and extrinsic conditions (Koutsoumanis et al., 1999). Inaddition, the effects of Zataria multiflora oil were determined in a foodmodel using different extrinsic conditions such as time and tempera-ture (Moosavy et al., 2008). The growth and the number of CFUs of S.Typhimurium were also reduced at significant level by using the oil ofZ. multiflora (Moosavy et al., 2008).

Findings have been observed regarding the efficacy of PEOs invivo, however, only few reports have confirmed the precise mode ofaction of PEOs in food models. To determine the effect of any specificPEO at any particular growth stage of bacteria can be a focal area ofresearch in order to visualize the adaptability of PEOs in any proposedfood model (Rees, Dodd, Gibson, Booth, & Stewart, 1995). However,as reported previously, modifications in the bacterial cell membranecomposition might result in susceptibility of the pathogen (Ultee &Smid, 2001). Besides, the cell rich in nutrient uptake survives betteras compared to the cell lasting in starving condition (Gill, Delaquis,Russo, & Holley, 2002). In addition, both intrinsic and extrinsic condi-tions can be responsible to the susceptibility or resistant nature of thepathogen (Juven et al., 1994; Shelef, 1983; Skandamis & Nychas,2000; Tassou, Drosinos, & Nychas, 1996; Tassou et al., 1995;Tsigarida et al., 2000). Besides, fatty contents may also serve as barrierto the effectiveness of the pathogen while incorporating PEO in foodsdue to having a higher population of pathogen in hydrophilic region(Mejlholm & Dalgaard, 2002; Smith-Palmer, Stewart, & Fyfe, 2001).Hence, it is assumed that fatty composition may directly have an ad-versary effect on the efficacy of PEOs against the tested pathogens.

In addition, interaction of terpenoid phenolics of PEOs with enzy-matic substances might be a reason to limit the antimicrobial efficacyof the PEOs in food models (Pol, Mastwijk, Slump, Popa, & Smid,2001; Smith-Palmer et al., 2001). It has been also known that food hy-drocarbons have less ability to control the killing effect of PEOsagainst pathogens as compared to the proteinous or fatty substances(Shelef, Jyothi, & Bulgarelli, 1984). Moreover, salt-content may also


influence the efficacy of PEOs in food models (Shelef et al., 1984;Skandamis & Nychas, 2000; Tassou et al., 1995; Wendakoon &Sakaguchi, 1993).

Food properties and several other abiotic and biotic factors mayinfluence the antimicrobial efficacy of PEOs (Skandamis et al.,

Table 1Minimum inhibitory (MIC) and bactericidal (MBC) concentrations of selected PEOs against

Essential oil derived from Bacteria MIC

Sphallerocarpus gracilis (seeds) Salmonella Typhimurium 320a

Salmonella Enteritidis 320a

Cesturm nocturnum (flower) S. Typhimurium 25.0a

Ziziphus jujuba (seed) S. Typhimurium 250a

Lonicera japonica (flower) S. Typhimurium 125a

S. Enteritidis 250a

Metasequoia glyptostroboides (leaf) S. Typhimurium 1000a

S. Enteritidis 1000a

Nandina domestica (flower) S. Typhimurium 500a


Syzygium aromaticum (bud) S. Typhimurium >2.0b

S. Enteritidis 80–320a

Thymus vulgaris (herb) S. Typhimurium 0.45–720

S. Enteritidis 66.7–320

Pogostemon patchouli (leaf) S. Typhimurium >2.0b

Prunus armeniaca (seed) S. Typhimurium >2.0b

Rosmarinus officinalis (herb) S. Typhimurium >2.0b

S. Enteritidis –

Cedrus atlantica (wood) S. Typhimurium >2.0b

Citrus aurantium (peel) S. Typhimurium >2.0b

Cleistocalyx operculatus (bud) S. Typhimurium 4000a


Silenea armeria (flower) S. Typhimurium 1000a


Magnolia liliflora (flower) S. Typhimurium 1000a

Pinus sylvestris (needles) S. Typhimurium >2.0b

Piper nigrum (berry) S. Typhimurium >2.0b

Allium sativum (bulb) S. Enteritidis 80–320a

Curcuma longa (root) S. Enteritidis 133.3–32Zingiber officinale (rhizome) S. Typhimurium >2.0b

Vetiveria zizanioides (leaf) S. Typhimurium >2.0b

Ostericum koreanum (leaf) S. Enteritidis (AR) 8–16b

S. Typhimurium (AR) 4–8b

Cymbopogon citratus (leaf) S. Enteritidis (AR) 0.5–8b

S. Typhimurium (AR) 0.5–8b


Mentha piperita (herb) S. Typhimurium 1.0b

S. Enteritidis –

Mentha spicata S. Typhimurium –

S. Enteritidis –

Ocimum basilicum (herb) S. Typhimurium 2.0b


Origanum vulgare (herb) S. Typhimurium 0.12–3.1

S. Enteritidis 66.7–160

Ferula assafoetida (seed) S. Typhimurium 145a

Poncirus trifoliata (seed) S. Enteritidis 250a

Prunus dulcis (seed) S. Typhimurium >2.0b

Salvia officinalis (herb) S. Typhimurium 2.0b

S. Enteritidis –

Salvia sclarea (herb) S. Typhimurium >2.0b

Santalum album (wood) S. Typhimurium >2.0b

Metasequoia glyptostroboides (cone) S. Typhimurium >2000a

S. Enteritidis >2000a

Citrus limon (peel) S. Typhimurium >2.0b

Cymbopogon citratus (leaf) S. Typhimurium 1.0b

S. Enteritidis 1.0b

Eucalyptus polybractea (leaf/twigs) S. Typhimurium 0.25b

Melaleuca alternifolia (leaf/twig) S. Typhimurium 0.5b

MIC: minimum inhibitory concentration; MBC: minimum bactericidal concentration.AR: antibiotic resistant pathogens.

a Represents MIC or MBC value in μg/ml.b Represent MIC or MBC value in μl/ml.

2000). Miscibility of the samples in liquid or solid phase can alsolimit the antimicrobial potential of PEOs (Hammer, Carson, & Riley,1999). We have immensely screened the biological efficacy of variousPEOs and evaluated their MIC values against Salmonella community.The MIC treated sample when inoculated on the agar media, showing

Salmonella spp. in vitro.

MBC Reference

320a Gao et al. (2011)640a

– Al-Reza, Rahman, and Kang (2009)– Al-Reza, Rahman, Lee, and Kang (2010)– Rahman, Lee, and Kang (2009b)–

– Bajpai, Al-Reza, Choi, Lee, and Kang (2009)–

– Bajpai et al. (2008)–

– Hammer et al. (1999)– Rattanachaikunsopon and Phumkhachorn (2010)

b 1.25b Hammer et al. (1999); Cosentino et al. (1999); Roldán,Díaz, and Duringer (2010);

a 0.625b Rattanachaikunsopon and Phumkhachorn (2010);Roldán et al. (2010)Hammer et al. (1999)Hammer et al. (1999)

40b Roldán et al. (2010); Hammer et al. (1999)40b Roldán et al. (2010)

Hammer et al. (1999)Hammer et al. (1999)

4000a Dung, Kim, and Kang (2008)4000a

– Bajpai, Dung, Kwon, and Kang (2008)–

– Bajpai, Rahman, Dung, Huh, and Kang (2008)Hammer et al. (1999)Hammer et al. (1999)

– Rattanachaikunsopon and Phumkhachorn (2010)0a – Rattanachaikunsopon and Phumkhachorn (2010)


– Shin (2005a)–

– Shin (2005b)–

– Rattanachaikunsopon and Phumkhachorn (2010)40b Roldán et al. (2010); Hammer et al. (1999)40b Roldán et al. (2010)10b Roldán et al. (2010)10b Roldán et al. (2010)5b Roldán et al. (2010); Hammer et al. (1999)10b Rattanachaikunsopon and Phumkhachorn (2010);

Roldán et al. (2010)2b 0.312b Derwich, Benziane, Manar, Boukir, and Taouil (2010);

Hammer et al. (1999); Roldán et al. (2010);a 0.078b Rattanachaikunsopon and Phumkhachorn (2010);

Roldán et al. (2010)– Rahman, Gul, and Dhano (2008)

Rahman, Al-Reza, Yoon, and Kang (2009a)Hammer et al. (1999)

40b Roldán et al. (2010); Hammer et al. (1999)80b Roldán et al. (2010)


– Bajpai, Rahman, Choi, and Kang (2007)– Hammer et al. (1999)– Hammer et al. (1999)– Hammer et al. (1999)

Raybaudi-Massilia et al. (2006)– Hammer et al. (1999)– Hammer et al. (1999)


no growth of target pathogen is known as minimum bactericidal con-centration (MBC). However, MIC differs in the research publications,which is another hurdle to compare the efficacy of test moleculeamong the researches (Burt, 2004; Hammer et al., 1999). A detaileddescription on antibacterial efficacy as MIC and MBC values of variousPEOs and their volatiles against Salmonella in food commodities isgiven in Tables 1 and 2, respectively.

2.5. Salmonella control in meat and poultry products

Certain PEOs and their volatiles may work as natural food preserva-tive compared to synthetic and chemical preservatives with less toxicity.Wrapping films have been used in corporation with PEOs or their vola-tiles in order to confirm their efficacy against Salmonella species in foodcommodities. The antimicrobial films along with PEOs or their volatileshave shown concentration-dependent activity in meat products,confirming the reduction of bacterial population at significant level(Ravishankar, Zhu, Olsen,McHugh, & Friedman, 2009). Current literaturesurvey on the efficacy of the PEO components has also confirmed theirefficacy to inhibit the growth of Salmonella bacteria up to a significant re-duction in the CFU levels (Ravishankar et al., 2010). The PEO volatiles eu-genol, trans-cinnamaldehyde, carvacrol, and thymol were tested againstSalmonella Enteritidis in chicken cecal contents, and reduced the CFUnumbers of target pathogen to an exceeding limit (Johny, Darre,Donoghue, Donoghue, & Venkitanarayanan, 2010). As reported previ-ously, the fatty contentsmight have essential role in reducing the activityof PEOs in food products (Gill et al., 2002; Tassou et al., 1995).

Govaris, Solomakos, Pexara, and Chatzopoulou (2010) visualized theefficacy of oregano PEO against the microbe of Salmonella species inmeat product, and it was found that the oil confirmed the acceptancelevel of organoleptical level. Besides, PEOs from Salvia officinalis andSchinus mollewere examined against pathogenic bacteria of Salmonellaspecies inmeat ormeat product (Hayouni et al., 2008). PEOs from S. offi-cinalis and S. molle were found to exhibit remarkable inhibitory effectagainst the tested pathogens with improved sensory properties and re-duced pattern of CFU numbers (Hayouni et al., 2008).

In another study conducted using PEOs of thyme and oregano in-corporating packaging strategy was evaluated in order to prolongthe quality of lamb meat (Karabagias, Badeka, & Kontominas, 2011).This study confirmed the marked efficacy of both PEOs in vivo and re-duced the pathogen load up to a significant level during storage ofmeat with improved organoleptic properties, confirming the use ofnatural antimicrobials in meat preservation (Karabagias et al., 2011).

Table 2Minimum inhibitory concentrations (MIC) of selected PEO components against Salmonella

Essential oil component Bacterial pathogens MIC

Eugenol Salmonella Typhimurium 0.012S. Typhimurium 0.5a

α-Pinene S. Typhimurium (AR) 8–16Salmonella Enteritidis (AR) 8a

α-Terpineol S. Typhimurium 0.225Carvacrol S. Typhimurium 0.225

S. Typhimurium 1 mMCitral S. Typhimurium 0.5a

Geraniol S. Typhimurium 0.5a

Perillaldehyde S. Typhimurium 0.5a

Thymol S. Typhimurium 0.056S. Typhimurium 1 mM

(+)-Carvone S. Typhimurium 10 mTrans-cinnamaldehyde S. Typhimurium 3 mMCinnamaldehyde Salomonella sp. 500b

MIC: minimum inhibitory concentration; AR: antibiotic resistant pathogens.a Values in μl/ml.b Values in μg/ml.

Several PEO components have been used to control the pathogenload in foods. Vapor phase effect of PEO component (carvacrol)was evaluated to limit the propagation of foodborne pathogen ofSalmonella species in meat or meat products (Burt, Fledderman,Haagsman, van Knapen, & Veldhuizen, 2007). It was confirmed inthe findings of this research that volatile compound was found tominimize the CFU numbers of target pathogen to an extended limit,and was able to maintain the shelf-life of meat produces significantly(Burt et al., 2007).

The addition, cinnamon bark PEO (7000 ppm) exerted the stron-gest antibacterial efficacy against Salmonella in liquid whole egg,being able to inhibit a population up to day 6. However, rosemaryPEO showed low antibacterial efficacy. The bioactive components ofcinnamon bark oil were found to inhibit the bacterial load to unde-tectable levels in egg white and whole egg. The efficacy of bioactiveprinciples of cinnamon bark PEO was also confirmed on the basis ofno changes found in °Brix with reduction in pH value. The physicalproperties of egg were also improved in liquid whole (Valverde etal., 2010).

The effect of defined concentration of PEO volatile (citral) wasconfirmed in fisheries products against S. Typhimurium with reducedlevel of CFU bacterial numbers (Kim, Marshall, Cornell, Preston, &Wei, 1995b).

2.6. Salmonella control in milk and dairy products

PEO from mint was evaluated against S. Enteritidis in milk prod-ucts, which was found to reduce the growth of microbial starter cul-ture load to a significant level. However, other volatiles includingthe PEOs from cinnamon, cardamom and clove were found highlyantibacterial against the tested foodborne pathogen in yogurt and cu-cumber commodities (Bayoumi, 1992; Tassou et al., 1995). In addi-tion, some of the PEO volatile components tested against Salmonellaconfirmed that only orange, lemon and grapefruit were found selec-tive to treat milk samples (Dabbah, Edwards, & Moats, 1970). Thesevariations on the antibacterial efficacy of the tested PEOs or volatilesmight occur due to the percentage of the fatty composition, whichlimits the killing action of the samples to the target pathogen(Holley & Patel, 2005). In addition, PEOs from clove, cinnamon, bayand thyme evaluated for their efficacy against Salmonella species ina food model of cheese showed similar pattern of antibacterial effica-cy due to the variations in the fatty composition (Smith-Palmer et al.,2001).

spp. in vitro.

(approximate range) References

5% Devi, Arif Nisha, Sakthivel, and Pandian (2010)Kim et al. (1995a)

a Shin (2005a)Shin (2005b)

a Cosentino et al. (1999)–0.25a Kim et al. (1995b); Cosentino et al. (1999)

Helander et al. (1998)Kim et al. (1995b)Kim et al. (1995b)Kim et al. (1995b)

a Cosentino et al. (1999)Helander et al. (1998)

M Helander et al. (1998)Helander et al. (1998)Chang, Chen, and Chang (2001)


2.7. Salmonella control in fruits, vegetables and juices

Salmonella bacteria have been isolated from a variety of herbal com-modities. Literature survey confirmed 8% incidence of Salmonella in veg-etables (Rude, Jackson, Bier, Sawyer, & Risty, 1984). Also it has beenreported that 7.5% incidences were found in Spain (Garcia Villanova-Ruiz, Galvez-Vargas, & Garcia-Villanova, 1987), and 9 to 10% incidenceswere reported in New Jersey (Wells & Butterfield, 1997). Ercolani(1976) found Salmonella on 68% of lettuce and 72% of fennel samples.Salmonella can be propagated on herbal commodities in the presenceof favorable conditions (Wells & Butterfield, 1997). Natural phytochem-icals such as PEOs or their volatiles have been used consistently to elim-inate bacterial populations on fruits and vegetables.

The potential of PEO volatiles against Salmonella species was evalu-ated in tomatomodel. The findings of this study confirmed that the PEOvolatiles significantly reduced themicrobial load of target pathogens ontomato samples to a limit of about 6.0 log10 CFU/ml (Mattson et al.,2011). It appeared that in vegetable dishes, the biological efficacy ofPEOs is attributed to both intrinsic and extrinsic properties of the sam-ple products (Skandamis &Nychas, 2000). Also the less fatty contents ofvegetables may influence the biological efficacy of the tested PEOs(Singh, Singh, Bhunia, & Stroshine, 2002; Wan et al., 1998). Some ofthe PEO volatiles inhibited Salmonella species in the foodmodel of alfal-fa seeds effectively (Weissinger, McWatters, & Beuchat, 2001).

The efficacy of myrtle PEO was evaluated against the antibiotic re-sistant pathogen of Salmonella species in food models of tomato andlettuce. Treatment with myrtle PEO significantly reduced the numberof microbial load on the tested food models with an expected countlimit (Gunduz, Gonul, & Karapinar, 2009). In another study, some ofthe plant volatiles such as carvacrol and cinnamaldehyde werefound to exert potent reduction rate in the CFU count of the targetpathogens in the food model of kiwi fruits, however, exerted a low in-hibitory effect in the food model of honeydew melon. These varia-tions might be correlated to the intrinsic or extrinsic properties ofthe foods (Roller & Seedhar, 2002).

The PEO from oregano was evaluated in order to confirm its bio-logical potential against Salmonella species in a food model of lettuce.These findings confirmed the marked efficacy of the PEO of oregano,hence has the ability to work as a natural alternative treatment tochemical washing solution in order to retain the quality of food prod-ucts contaminated by foodborne pathogenic bacteria (Gunduz, Gonul,& Karapınar, 2010a).

In addition to this, the antimicrobial efficacy of oregano PEO eval-uated against the species of resistant Salmonella on tomato foodmodel confirmed that oregano PEO was found effective against thetest resistant pathogen of Salmonella, and significantly reduced the vi-able count numbers at the level of 2.78 logarithms in tomato foodmodel (Gunduz, Gonul, & Karapınar, 2010b).

The orange PEO without terpene was evaluated against Salmonellaspecies, and provoked significant results on the antibacterial efficacyin juice model, reducing the population of target pathogen to a desir-able limit (Parish, Baum, Kryger, Goodrich, & Baum, 2003). In order toconfirm the potential of lemongrass and geraniol volatiles against thepathogens belonging to genus Salmonella, non-treated juices fromapple, pear and lemon fruits were examined. Both PEOs were foundeffective to inhibit the population of target pathogens to a limit of3 log10 CFU/ml in juice models (Raybaudi-Massilia et al., 2006). A lit-erature description on the applicable efficacy of PEOs and their vola-tiles in food system has been summarized in Table 3.

3. Applications of PEOs in food packaging

PEO-based antimicrobial packagings serve as potent antimicrobialstrategies to inhibit the propagation of foodborne pathogens in a de-sired food model. A number of PEOs and their volatiles were found topossess significant impact on the antimicrobial efficacy in food

packaging systems, which are the natural sources to serve as potentantimicrobials in food preservation technology (Cagri, Ustunol, &Ryser, 2004; Min, Harris, Han, & Krochta, 2005; Tharanathan, 2003).

In spite of new insights in chemical preservation, concern hasbeen raised in regard not to using chemical preservatives in food sys-tem to prolong the shelf-life of food produces except natural antimi-crobials. However, contamination free food or food products havebeen in demand in recent time in order to diminish foodborne ill-nesses to human safety caused by foodborne pathogens. This hasresulted in the emergence of enormous issues to secure the food safe-ty from chemical preservation with no harmful effect to consumers(Vermeiren, Devlieghere, van Beest, de Kruiif, & Debevere, 1999).

Food packaging strategies using natural antimicrobials could be asafe alternative in food preservation technology. Natural antimicro-bials as packaging food preservative stuffs with enhanced biologicalefficacy are very much in demand in recent time to maintain the pro-longed life of perishable food produces (Matan et al., 2006; Suppakul,Miltz, Sonneveld, & Bigger, 2006).

Recently, the packaging films containing natural antimicrobialshave been used extensively to maintain the shelf-life of the packedfood produces (Iseppi et al., 2008; Miltz, Rydlo, Mor, & Polyakov,2006; Plackett & Ghambari-Siahkali, 2007). In fact, the antimicrobialefficacy of PEOs has been well-known from the last many yearsusing PEOs in food packaging actively (Gutierrez, Sanchez, Batlle, &Nerin, 2009; Lopez, Sanchez, Batlle, & Nerın, 2007; Matan et al.,2006; Rodriguez, Nerın, & Batlle, 2008). The use of PEOs and their vol-atiles for their practical applications as packaging material could be aunique feature in order to maintain the food safety (Gutierrez et al.,2009).

The active PEO volatiles during the preservation of food stuffswork consistently to make the foods free from microbial load and re-duce their population by contact methodology (Gutierrez et al., 2009;Quintavalla & Vicini, 2002). Besides, incorporation of PEOs or theirvolatiles with polymer molecules can be a good strategy in food pres-ervation technology to limit the propagation of foodborne pathogens(Appendini & Hochkiss, 2002; Oussallah, Caillet, Salmieri, Saucier, &Lacroix, 2004).

Natural herbal spices possess rich amount of phenolics which exertstrong antimicrobial efficacy both in vitro and in vivo (Dadalioglu &Evrendilek, 2004; Seydim& Sarikus, 2006). Almost all the PEOs showingbiological efficacy against foodborne pathogens possess higher amountof phenolic contents which also include carvacrol, eugenol and thymol(Burt, 2004; Seydim & Sarikus, 2006). According to Seydim andSarikus (2006), whey protein films incorporating bioactive volatiles,were found to serve as better antimicrobials against the Salmonellaspecies.

In some cases, practical use of PEOs in food preservation can dete-riorate the food quality, hence, the use of PEOs in packaging films can-not give the positive results in case of some specific food product,thus can be considered of secondary use. Although, PEOs applicationto the packaging industry can be beneficial in food preservation, fur-ther confirmatory trials are still needed to confirm their practical ap-plication for food preservation. Previous reports on the efficacy oforegano PEO as bioactive material in other types of packaging filmshave confirmed the potential of PEOs or their volatiles (Dadalioglu& Evrendilek, 2004).

On the other hand, efficacy of selected combinations of severalother PEOs comprising irradiation technique has been confirmed inmeat or food products to minimize the microbial load of foodbornepathogens as well as to visualize the impact of such combinationson the quality of meat products (Turgis, Han, Borsa, & Lacroix, 2008).

4. Application of PEOs or their components in poultry

Salmonella can cause septicemic diseases in poultry. Exposure ofSalmonella to broilers can cause stomach disorders and can prolong

Table 3In vivo antibacterial activity of selected PEOs or their components against Salmonella spp. in foods.

Food group Food type Essential oil or component Concentrationapplied

Bacterial pathogens Observations References

Meat or poultryproducts

Fresh lamb meat Thyme or oregano oil 0.1 or 0.3% Salmonella 4 °C, MAP2 found more effective Karabagias et al. (2011)Minced sheep meat Oregano oil 0.6 or 0.9% Salmonella Enteritidis Higher organoleptical attributes at 0.6% at 10 °C Govaris et al. (2010)Chicken cecal trans-cinnamaldehyde, eugenol,

carvacrol, and thymol10–75 mM S. Enteritidis At 40 °C/log reduction (6.0 to >8.0) Johny et al. (2010)

Chicken heart Cinnamaldehyde or carvacrol 0.5–3% Salmonella Enterica At 23 °C/log reduction (6.8 to 1.6) At 4 °C/logreduction (3.0 to 0.8)

Ravishankar et al. (2009)

Minced beef meat Salvia officinalis and Schinus molle oils 0.02, 0.06, 0.1, 1,1.5, 2, and 3%

S. Anatum A large reduction ranged: 1 to 3 CFU/ml or g, or fewer Hayouni et al. (2008)S. Enteritidis

Liquid whole egg Cinnamon bark essential oil 7000 ppm Salmonella sp. Reduction about 102 CFU/ml Valverde et al. (2010)Chicken noodles Sage oil 200–500 ppm S. Typhimurium Slight reduction up to 1.5 log CFU/ml or g Shelef et al. (1984)Pieces of raw chicken Carvacrol 20–100% S. enterica serotype Enteritidis Complete inhibition of log CFU at 40% Burt et al. (2007)Pate Mint oil 0.5 to 2.0% S. Enteritidis Negligible effect Tassou et al. (1995)

Fruits, vegetables,and juices

Celery Cinnamaldehyde or carvacrol 1% S. Newport Complete reduction in CFU by 1% carvacrol;1–2.3 log reduction by 1% cinnamaldehyde

Ravishankar et al. (2010)

Plum tomato Carvacrol, trans-cinnamaldehyde,eugenol, and β-resorcylic acid

0.25–1% Salmonella sp. Reduction in log CFU about 6.0 Mattson et al. (2011)

Tomato and shreddediceberg lettuce

Myrtus communis leaf essentialoil

1000 ppm S. Typhimurium Reduction in log CFU about 1.66 and 1.89 Gunduz et al. (2009)

Iceberg lettuce Oregano oil 25, 40, 75 ppm S. Typhimurium Significant log reduction at 75 ppm Gunduz et al. (2010a)Tomato Oregano oil 15, 75, 100 ppm Nalidixic acid resistant S. Typhimurium Log reduction about 2.78 Gunduz et al. (2010b)Kiwifruit Carvacrol 1 mM (dipping

solution)Natural flora A large reduction about: >3 log CFU/ml

or g, or fewerRoller and Seedhar (2002)

Alfalfa seeds Cinnamaldehyde, thymol 200, 600 mg/l, air Salmonella spp., (6 serotypes) Reduction about: negligible to 1.5 log CFU/mlor g or fewer

Weissinger et al. (2001)

Cucumber salad Mint oil 0.5–2.0% S. Enteritidis Tassou et al. (1995)Apple, pear and melonjuices

Lemongrass or geraniol – Salmonella 3 log CFU reduction in apple juice Raybaudi-Massilis et al.(2006)

Grain Barley soup Zataria multiflora oil 0–100 μl/ml S. Typhimurium Significant log reduction Moosavy et al. (2008)Boiled rice Sage oil 200–500 ppm S. Typhimurium Negligible effect on log CFU reduction Shelef et al. (1984)

Fish or fishproducts

Red grouper filet,cubed

Carvacrol, citral, geraniol 0.5–3.0% (dippingsolution)

S. Typhimurium Reduction about: 1.5–3.0 or up to 1.5 CFU/ml or g Kim et al. (1995b)

Taramasalad (cod's rocsalad)

Oregano oil 0.5–2.0% S. Enteritidis A large reduction about: >3 log CFU/ml or g or fewer Koutsoumanis et al. (1999)

Milk or dairyproducts

Pasteurized milk Terpineol or orange oil 100 ml/l Salmonella Terpineol most effective, a large reduction about:7 log in skimmed milk, 4 log in low butterfatmilk and 3 log in whole milk

Dabbah et al. (1970)

Tzatziki (Yogurt) Mint oil 0.5–2.0% S. Enteritidis Tassou et al. (1995)

729V.K.Bajpaiet

al./Food

ResearchInternational45

(2012)722

–734


the shedding. Severity of the disease can increase the death rate ofthe chickens. Efficacy of the virulence-strain can spread the diseasesymptom to the other body sites, which can cause the infection inthe eggs to be laid. The infection by Salmonella in chicken or broilershas been reported previously (Jamshidi, Bassami, & Afshari-Nic,2008). Although, a number of serovars of Salmonella have beenreported from poultry chickens, virulence efficacy of all the Salmonel-la has not been found to infect human beings.

PEOs available in market for animal production use are known toplay a significant role in digestive system (Williams & Losa, 2001).Based on biological efficacy of PEOs, consideration can be made on thepractical applications of PEOs as prophylactic and therapeutic agents.The intake of PEOs affects the gastrointestinal microflora compositionand population. Previous investigations on the antibacterial activity ofvarious PEOs have confirmed the potent efficacy of several PEOs on coc-cidia oocyte output and the number of bacteria in broiler chicks whenartificially inoculated (Evans, Plunkett, & Banfield, 2001). Marketableformulations of PEOs were given as diet supplements. This preparationindicated the antimicrobial activity in broilers (Smits, Veldman,Verstegen, & Beynen, 1997; Veldman & Enting, 1996). It was reportedthat dietary carvacrol versus thymol reduced the animalweight and nu-tritional intake, but improvements were observed in broilers when fedwith their respective diet for 4 weeks (Lee, Everts, Kappert, Yeom, &Beynen, 2003). Thus, it might be concluded that PEOsmay act on intes-tinal microflora as well as on nutrient utilization.

Ordonez, Llopis, and Penalver (2008) reported the potent antibacter-ial activity of Eugenia caryophyllata PEO against Salmonella bacteria in fe-male chicken model. The PEO derived from E. caryophyllata containingrich amount of volatile eugenol served as better disinfectant whilesacrificing the hens. Also the use of volatile was helpful to prevent theegg contamination caused by Salmonella species (Ordonez et al., 2008).

The characteristic flavor of PEOs may function in poultry. PEOs canalso enhance the functional activity of digestive system. Besides, PEOvolatiles can also exert diverse roles of action as additive, synergisticand antagonistic patterns, when applied individually. The PEOs withwell known chemical nature can provide indepth insights for theirpractical applications in poultry management.

5. Synergism and antagonism between oil components

The antibacterial efficacy of PEOs can be attributed to the volatilemajority of PEO; volatile ratio as well as their behavior of mode of ac-tion (Burt, 2004; Delaquis et al., 2002; Dorman & Deans, 2000; Marinoet al., 2001). Antagonistic efficacy can be visualized upon the supplyof two compounds where the sample mixture has low antimicrobialefficacy as compared to using them separately (Burt, 2004). Addition-al antimicrobial efficacy can be visualized upon the supply of twocompounds where the sample mixture has similar antimicrobial effi-cacy while using them separately (Burt, 2004). However, when com-binatory effect of compounds is higher than the effect of individuals isknown as synergism (Burt, 2004; Davidson & Parish, 1989). Literaturesurvey has demonstrated that an oil as a whole showed better anti-bacterial efficacy than only a combination of major volatiles of theoil (Burt, 2004; Gill et al., 2002; Mourey & Canillac, 2002). Hence, itmight be said that the minor elements of the oil have crucial rolesto increase the biological effectiveness of the oil, resulting in the syn-ergism (Burt, 2004). We reported that cone PEO of Metasequoia glyp-tostroboides exerted potential synergistic effect with nisin againstGram-positive bacteria at varied concentrations in whole, low andskimmilks (Yoon, Bajpai, & Kang, 2011). Combined fractions of differ-ent PEOs such as cilantro, coriander, dill and eucalyptus have beenshown to exert synergistic and additive mode of action (Burt, 2004;Delaquis et al., 2002). Although, proportions of volatile compoundsof PEOs have been found to exhibit a complete inhibitory action onsome of the foodborne pathogens, however, these volatiles couldnot be able to exert antibacterial efficacy when applied individually

against the tested organisms (Burt, 2004; Moleyar & Narasimham,1992). The efficacy of Z. multiflora PEO with a known chemical preser-vative was evaluated against S. Typhimurium in a food model(Moosavy et al., 2008). The growth of S. Typhimurium was reducedby the addition of the mixture sample of oil and chemical preserva-tive (nisin). The biological efficacy of PEOs not only corresponds tothe volatiles present in a higher quantity but also the volatiles presentin low amount can influence the biological efficacy of whole PEO. An-alyzing the chemical compositions of PEOs shows significant quanti-tative differences in the oil components.

6. Laws and regulations on the use of PEOs in foods

The European Union (EU) is constantly producing themost valuablerecommendations and laws for using plant volatiles and PEOs in foodsystem to retain the quality of the food or food products which are eas-ily hampered by the foodborne pathogenic bacteria. FDA is very likely tofollow the EU over these issues. Several PEOs and volatiles in their mar-ketable forms are sold as flavoring agents to enhance the longevity offood produces (Burt, 2004). The registration of oil or oil componentsat EU or FDA is considered the products to be non-hazardous as wellas safe to the health of consumers which include allspice oil, anise oil,black pepper oil, caraway oil, cubeb oil, star anise oil, sweet bay oiland thymol etc. (Burt, 2004). On especial recommendations, some ofthe component substances have been black-listed because of their gen-otoxic effects (Burt, 2004; Commission Decision of 23 January, 2002).Besides, a new registration to serve as a flavoring agent can only be con-sidered by the commission if the concernedmetabolic and toxicologicalresearch has been performed (Commission Decision of 23 February,1999; Commission Regulation (EC) No 1565/2000 of 18 July, 1565/2000; Commission Regulation (EC) No. 622/2002 and Regulation (EC)No 2232/96; Burt, 2004).

According to Burt (2004), the flavoring agents which have registeredat EU have also been used by the USA people for their daily purposeneeds (http://www.cfsan.fda.gov/˜dms/eafus.html, date consulted: 26February 2003). Hence, these substances are classified as approvedfood additives (Burt, 2004; Smoley, 1993). Although, estragole hasbeen prohibited to include in the list of EU as flavoring, however, furtherrecommendations have been made for its safe utilization (Burt, 2004).

The PEOs or volatiles might be considered as new food additives ifthey are added to food or food stuffs for the purpose other than servingas flavoring agents (Burt, 2004). However, to serve these substances asfood additiveswill certainly require to carrying out the studies on safetyand toxicology as well as metabolic profiling. Interestingly, it will bemore beneficial economically to the people of the developing countriesto use herbal plant or the plant parts as a whole or a whole PEO as aningredient as well as herbal drug than using an individual componentof the PEO (Burt, 2004; Smid & Gorris, 1999).

7. Future perspectives

The most diverse and interesting area of PEOs and their volatilesfor their proper utilization is to suppress hazardous pathogens includ-ing Salmonella species. The improvement in the quality of packedmeat or food products as well as spoilage delay by food spoilage orfoodborne pathogens might be an important area of further research.Organoleptic properties may encounter another area where the PEOscan be easily incorporated in food products (Burt, 2004). The PEOscan also be used in the food stuffs which have not been associatedpreviously with any flavor, if one or more components of the oil to-gether can exert the desired antibacterial efficacy at the particularamount, having no deteriorating effect on the organoleptic or sensoryproperties of food products (Burt, 2004).

In fact, the consumer goods are experiencing an increased influ-ence of PEOs or their volatiles in order to develop new and effectivenatural antimicrobials of plant origin (Burt, 2004; Tuley de Silva,

http://www.cfsan.fda.gov/~dms/eafus.html


1996). These products can also be served as natural in other relatedindustries for their safe use (Bassett, Pannowitz, & Barnetson, 1990;Burt, 2004). For large scale production of PEOs, biotechnological ap-proaches of their synthesis may be useful to obtain the desired vol-ume of PEOs (Burt, 2004; Mahmoud & Croteau, 2002; McCaskill &Croteau, 1999). In addition, standardization of the chemical natureof commercial PEOs will be needed for their safe and practical appli-cations (Burt, 2004; Carson & Riley, 2001).

The mechanism role of PEOs and volatiles on proteins associatedwith cytoplasmic membrane as well as on lipid structure has notbeen completely studied; hence, it might be an important aspect offuture studies (Burt, 2004). Moreover, evaluation of the mechanismof action of PEOs will potentially strengthen their practical applica-tions and significance in future research (Burt, 2004).

In addition to this, research findings on the interactions betweenPEOs and their components as well their effect as food ingredientsor food additives also require further investigation (Burt, 2004). Inorder to optimize the antibacterial efficacy, synergistic, antagonisticand additive effects of PEOs can be explored so as to optimize thelowest concentration required for the inhibition of any food spoilageor foodborne pathogenic bacteria which will indeed be a helpful strat-egy in the practical application of PEO in the future (Burt, 2004).

Also to measure the stability of PEOs and their volatiles duringfood processing might be a focal area of future research (Burt,2004). Besides, experimental data on various direct or indirect conse-quences of using PEOs and their volatiles will confirm whether thePEO or its volatiles are safe to use in the food industry (Burt, 2004).

8. Conclusion

Salmonella is one of the major foodborne pathogens. Food or foodproduces are the major Salmonella sources to cause the foodbornediseases. Practical applications of PEOs are needed for the completeelimination of foodborne pathogens. Several PEOs and their volatileshave shown a great deal to exert antimicrobial efficacy in foodmodel or food system to control foodborne pathogenic bacteria. Thevolatiles of PEOs from terpene origin are most likely to affect on themembrane permeability of target foodborne pathogen. Based on se-lectivity and specificity of foods, PEOs or their volatiles can be appliedto avoid the undesired effects of foodborne pathogens on the organo-leptic or sensory properties of food products. However, to furtherconfirm the safety of foods using PEOs or their volatiles, study ontheir safety issues must be conducted.

Acknowledgments

Thisworkwas carried outwith the support of “Cooperative ResearchProgram for Agriculture Science & Technology Development (ProjectNo. PJ007512)” Rural Development Administration, Republic of Korea.

References

Al-Reza, S. M., Rahman, A., & Kang, S. C. (2009). Chemical composition and inhibitoryeffect of essential oil and organic extracts of Cestrum nocturnum L. on food-bornepathogens. International Journal of Food Science and Technology, 44, 1176–1182.

Al-Reza, S. M., Rahman, A., Lee, J. G., & Kang, S. C. (2010). Potential roles of essential oiland organic extracts of Zizyphus jujuba in inhibiting food-borne pathogens. FoodChemistry, 119, 981–986.

Angioni, A., Barra, A., Cereti, E., Barile, D., Co sson, J. D., Arlorio, M., et al. (2004). Chem-ical composition, plant genetic differences, antimicrobial and antifungal activity in-vestigation of the essential oil of Rosmarinus officinalis L. Journal of Agricultural andFood Chemistry, 52, 3530–3535.

Appendini, P., & Hochkiss, J. H. (2002). Review of antimicrobial food packaging. InnovativeFood Science & Emerging Technologies, 3, 113–126.

Bajpai, V. K., Al-Reza, S. M., Choi, U. K., Lee, J. H., & Kang, S. C. (2009). Chemical compo-sition, antibacterial and antioxidant activities of leaf essential oil and extracts ofMetasequoia glyptostroboides Miki ex Hu. Food and Chemical Toxicology, 47(8),1876–1883.

Bajpai, V. K., Dung, N. T., Kwon, O. J., & Kang, S. C. (2008). Analysis and the potential ap-plications of essential oil and leaf extracts of Silene armeria L. to control food

spoilage and food-borne pathogens. European Food Research and Technology, 227,1613–1620.

Bajpai, V. K., Rahman, A., Choi, U. K., & Kang, S. C. (2007). Inhibitory parameters ofthe essential oil and various extracts of Metasequoia glyptostroboides Miki exHu to reduce food spoilage and food-borne pathogens. Food Chemistry, 105(3),1061–1066.

Bajpai, V. K., Rahman, A., Dung, N. T., Huh, M. K., & Kang, S. C. (2008). In vitro Inhibitionof food spoilage and food-borne pathogenic bacteria by essential oil and leaf ex-tracts of Magnolia liliflora Desr. Journal of Food Science, 73(6), 314–320.

Bajpai, V. K., Rahman, A., & Kang, S. C. (2008). Chemical composition and inhibitory pa-rameters of essential oil and extracts of Nandina domestica Thunb. to control food-borne pathogenic and spoilage bacteria. International Journal of Food Microbiology,125, 117–122.

Bakkali, F., Averbeck, S., Averbeck, D., & Idaomar, M. (2008). Biological effects of essen-tial oils — A review. Food and Chemical Toxicology, 46, 446–475.

Barbosa, L. N., Rall, V. L. M., Fernades, A. A. H., Ushimaru, P. L. I., da silva Probst, I.,Fernandes, A., et al. (2009). Essential oils against foodborne pathogens and spoilagebacteria in minced meat. Foodborne Pathogens and Disease, 6, 725–728.

Bassett, I. B., Pannowitz, D. L., & Barnetson, R. S. C. (1990). A comparative study of tea-treeoil versus benzoylperoxide in the treatment of acne. Medical Journal of Australia, 153,455–458.

Batlle, R., Colmsjo, A., & Nilsson, U. (2001). Determination of gaseous toluene diisocya-nate by use of solid-phase microextraction with on-fiber derivatisation. Fresenius'Journal of Analytical Chemistry, 369, 524–529.

Bauer, K., & Garbe, D. (1985). Common fragrance and flavor materials. Preparation,properties and uses (pp. 213). Weinheim: VCH Verlagsgesellschaft.

Bayoumi, S. (1992). Bacteriostatic effect of some spices and their utilization in themanufacture of yogurt. Chemie Mikrobiologie Technologie der Lebensmittel, 14,21–26.

Benkeblia, N. (2004). Antimicrobial activity of essential oil extracts of various onions(Allium cepa) and garlic (Allium sativum). Lebensm-Wiss u Technology, 37, 263–268.

Board, R. G., & Gould, G. W. (1991). Future prospects. In N. J. R. a. G. W. Gould (Ed.),Food preservatives (pp. 267–284). Glasgow: Blackie.

Botsoglou, N. A., Govaris, A., Botsoglou, E. N., Grigoropoulou, S., & Papageorgiou, G.(2003). Antioxidant activity of dietary oregano essential oil and α-tocopheryl ace-tate supplementation in long-term frozen stored turkeymeat. Journal of Agriculturaland Food Chemistry, 2003(51), 2930–2936.

Boyle, W. (1955). Spices and essential oils as preservatives. The American Perfumer andEssential Oil Review, 66, 25–28.

Burt, S. A. (2004). Essential oils: Their antibacterial properties and potential applica-tions in foods—A review. International Journal of Food Microbiology, 94, 223–253.

Burt, S. A., Fledderman, M. J., Haagsman, H. P., van Knapen, F., & Veldhuizen, E. J. A.(2007). Inhibition of Salmonella enterica serotype Enteritidis on agar and rawchicken by carvacrol vapor. International Journal of Food Microbiology, 119,346–350.

Burt, S. A., & Reinders, R. D. (2003). Antimicrobial activity selected plant essential oilsagainst Escherichia coli O157:H7. Letters in Applied Microbiology, 36, 162–167.

Caccioni, D. R. L., Guizzardi, M., Biondi, D. M., Renda, A., & Ruberto, G. (1998). Relation-ship between volatile components of citrus fruit essential oils and antimicrobialaction on Penicillium digitatum and Penicillium italicum. International Journal ofFood Microbiology, 43, 73–79.

Cagri, A., Ustunol, Z., & Ryser, E. T. (2004). Antimicrobial edible films and coatings. Journalof Food Protection, 67(4), 833–848.

Carson, C. F., Mee, B. J., & Riley, T. V. (2002). Mechanism of action of Melaleuca alterni-folia (tea tree) oil on Staphylococcus aureus determined by time-kill, lysis, leakageand salt tolerance assays and electron microscopy. Antimicrobial Agents and Che-motherapy, 46(6), 1914–1920.

Carson, C. F., & Riley, T. V. (1995). Antimicrobial activity of the major components ofthe essential oil of Melaleuca alternifolia. The Journal of Applied Bacteriology, 78,264–269.

Carson, C. F., & Riley, T. V. (2001). Safety, efficacy and provenance of tea tree (Melaleucaalternifolia) oil. Contact Dermatitis, 45, 65–67.

Chang, S. T., Chen, P. F., & Chang, S. C. (2001). Antibacterial activity of leaf essential oilsand their constituents from Cinnamomum osmophloeum. Journal of Ethnapharma-cology, 77(1), 123–127.

Chen, Y., & Pawliszyn, J. (2003). Time-weighted average passive sampling with a solid-phase microextraction device. Analytical Chemistry, 75, 2004–2010.

Commission Decision of 23 February (1999) adopting a register of flavouring sub-stances used in or on foodstuffs drawn up in application of Regulation (EC) No2232/96 of the European Parliament and of the Council on 28 October 1996.1999/217/EC: Official Journal L084, 27/03/1999, pp. 1–137.

Commission Decision of 23 January (2002) amending Commission Decision1999/217/EC as regards the register of flavouring substances used in or on food-stuffs. 2002/113/EC: Official Journal L49 20/02/2002, pp. 1–160.

Commission Regulation (EC) No 1565/2000 of 18 July (2000) laying down the mea-sures necessary for the adoption of an evaluation programme in application of Reg-ulation (EC) No 2232/96 of the European Parliament and of the Council: OfficialJournal L180 19/07/2000, pp. 8–16.

Commission Regulation (EC) No. 622/2002 of 11 April (2002) establishing deadlinesfor the submission of information of chemically defined flavouring substancesused in or on foodstuffs: Official Journal L95 12/04/2002, pp. 10–11.

Conner, D. E. (1993). Naturally occurring compounds. In P. Davidson, & A. L. Branen(Eds.), Antimicrobials in foods (pp. 441–468). New York: Marcel Dekker Inc.

Cosentino, S., Tuberoson, C. I. G., Pisano, B., Satta, M., Mascia, V., Arzedi, E., et al. (1999).In vitro antimicrobial activity and chemical composition of Sardinian Thymus es-sential oils. Letters in Applied Microbiology, 29, 130–135.


Cox, S. D., Mann, C. M., Markham, J. L., Bell, H. C., Gustafson, J. E., Warmington, J. R., et al.(2000). The mode of antimicrobial action of essential oil of Melaleuca alternifola(tea tree oil). Journal of Applied Microbiology, 88, 170–175.

Cutter, C. N. (2000). Antimicrobial effect of herb extracts against Escherichia coli O157:H7, Listeria monocytogenes, and Salmonella Typhimurium associated with beef.Journal of Food Protection, 63(5), 601–607.

Dabbah, R., Edwards, V. M., & Moats, W. A. (1970). Antimicrobial action of some citrusfruit oils on selected food-borne bacteria. Applied Microbiology, 19(1), 27–31.

Dadalioglu, I., & Evrendilek, G. (2004). Chemical compositions and antibacterial effectsof essential oils of Turkish oregano (Origanum minutiflorum), bay laurel (Laurusnobilis), Spanish lavender (Lavandula stoechas L.), and fennel (Foeniculum vulgare)on common foodborne pathogens. Journal of Agriculture and Food Chemistry, 52,8255–8260.

Davidson, P. M. (1997). Chemical preservatives and natural antimicrobial compounds.In M. P. Doyle, L. R. Beuchat, & T. J. Mont-Ville (Eds.), Food microbiology fundamen-tals and frontiers (pp. 520–556). ASM Press.

Davidson, P. M., & Parish, M. E. (1989). Methods for testing the efficacy of food antimi-crobials. Food Technology, 43, 148–155.

Deans, S. G., & Ritchie, G. (1987). Antibacterial properties of plant essential oils. Inter-national Journal of Food Microbiology, 5, 165–180.

Deans, S. G., & Sbodova, K. P. (1990). The antimicrobial properties of marjoram (Origa-num majorana L.) volatile oil. Flavour and Fragrance Journal, 5, 187–190.

Delaquis, P. J., Stanich, K., Girard, B., & Mazza, G. (2002). Antimicrobial activity of indi-vidual and mixed fractions of dill, cilantro, coriander and eucalyptus essential oils.International Journal of Food Microbiology, 74, 101–109.

Denyer, S. P., & Hugo, W. B. (1991). Biocide-induced damage to the bacterial cyto-plasmic membrane. In S. P. Denyer, & W. B. Hugo (Eds.), Mechanisms of actionof chemical biocides. The Society for Applied Bacteriology, Technical Series, No 27.(pp. 171–188) Oxford: Oxford Blackwell Scientific Publication.

Derwich, E., Benziane, Z.,Manar, A., Boukir, A., & Taouil (2010). Phytochemical analysis andin vitro antibacterial activity of the essential oil of Origanum vulgare from Morocco.American–Eurasian Journal of Scientific Research, 5(2), 120–129.

Devi, K. P., Arif Nisha, S., Sakthivel, R., & Pandian, S. K. (2010). Eugenol (an essential oilof clove) acts as an antibacterial agent against Salmonella Typhi by disrupting thecellular membrane. Journal of Ethanopharmacology, 130(1), 107–115.

Didry, N., Dubreuil, L., & Pinkas, M. (1993). Activite antimicrobienne du thymol, du car-vacrol et de l'aldehyde cinnamique seuls ou associes (Antibacterial activity of thy-mol, carvacrol, and cinnalmaldehyde singly or in combinations). Die Pharmazie, 48,301–308.

Dorman, H. J. D., & Deans, S. G. (2000). Antimicrobial agents from plants: Antibacterialactivity of plant volatile oils. Journal of Applied Microbiology, 88, 308–316.

Dung, N. T., Kim, J. M., & Kang, S. C. (2008). Chemical composition, antimicrobial andantioxidant activities of the essential oil and the ethanol extract of Cleistocalyxoperculatus (Roxb.) Merr and Perry buds. Food and Chemical Toxicology, 46,3632–3639.

EFSA (2009). The community summary report on trends and sources of zoonoses andzoonotic agents in the European Union in 2007, 20th January 2009. The EFSA Journal,223, 1–217.

El-Gazzar, E. F., & Marth, E. H. (1992). Salomonellae, Salmonellosis, and dairy foods: Areview. Journal of Dairy Science, 75, 2327–2343.

Ercolani, G. L. (1976). Bacteriological quality assessment of fresh marketed lettuce andfennel. Applied and Environmental Microbiology, 31, 847–852.

Evans, J. W., Plunkett, M. S., & Banfield, M. J. (2001). Effect of an essential oil blend oncoccidiosis in broiler chicks. Poultry Science, 80, 258.

Exarchou, V., Nenadis, N., Tsimidou, M., Gerothanassis, I. P., Troganis, A., Boskou, D.,et al. (2002). Antioxidant activities and phenolic composition of extracts fromGreek oregano, Greek sage, and summer savory. Journal of Agriculture and FoodChemistry, 50, 5294–5299.

Farag, R. S., Daw, Z. Y., Hewedi, F. M., & El-Baroty, G. S. A. (1989). Antimicrobial activityof some Egyptian spice essential oils. Journal of Food Protection, 52(9), 665–667.

Fisher, K., & Phillips, C. (2008). Potential antimicrobial uses of essential oils in food: Iscitrus the answer? Trends in Food Science and Technology, 19(3), 156–164.

Gao, C., Tian, C., Lu, Y., Xu, J., Luo, J., & Guo, X. (2011). Essential oil composition and an-timicrobial activity of Sphallerocarpus gracilis seeds against selected food-relatedbacteria. Food Control, 22, 517–522.

Garcia Villanova-Ruiz, B., Galvez-Vargas, R., & Garcia-Villanova, R. (1987). Contamina-tion of fresh vegetables during cultivation and marketing. International Journal ofFood Microbiology, 4, 285–291.

Gibson, A. M., Bratchell, N., & Roberts, T. A. (1988). Predicting microbial growth: Growthresponses of salmonellae in a laboratory medium as affected by pH, sodium chlorideand storage temperature. International Journal of Food Microbiology, 6, 155–178.

Gill, A. O., Delaquis, P., Russo, P., & Holley, R. A. (2002). Evaluation of antilisterial actionof cilantro oil on vacuum packed ham. International Journal of Food Microbiology,73, 83–92.

Gould, G. W. (1996). Industry perspectives on the use of the natural antimicrobials andinhibitors for food applications. Journal of Food Protection, 38, 82–86.

Govaris, A., Solomakos, N., Pexara, A., & Chatzopoulou, P. S. (2010). The antimicrobialeffect of oregano essential oil, nisin and their combination against SalmonellaEnteritidis in minced sheep meat during refrigerated storage. International Journalof Food Microbiology, 137, 175–180.

Guenther, E. (1948). The essential oils. New York. USA: D. Van Nostrand.Gunduz, G. T., Gonul, S. A., & Karapinar, M. (2009). Efficacy of myrtle oil against Salmo-

nella Typhimurium on fresh produce. International Journal of Food Microbiology,130, 147–150.

Gunduz, G. T., Gonul, S. A., & Karapınar, M. (2010). Efficacy of oregano oil in the inacti-vation of Salmonella Typhimurium on lettuce. Food Control, 21, 513–517.

Gunduz, G. T., Gonul, S. A., & Karapınar, M. (2010). Efficacy of sumac and oregano in theinactivation of Salmonella Typhimurium on tomatoes. International Journal of FoodMicrobiology, 141, 39–44.

Gustafson, J. E., Liew, Y. C., Chew, S., Markham, J. L., Bell, H. C., Wyllie, S. G., et al. (1998).Effects of tea tree oil on Escherichia coli. Letters in Applied Microbiology, 26,194–198.

Gutierrez, L., Sanchez, C., Batlle, R., & Nerin, C. (2009). New antimicrobial active pack-age for bakery products. Trends in Food Science and Technology, 20(2), 92–99.

Hammer, K. A., Carson, C. F., & Riley, T. V. (1999). Antimicrobial activity of essential oilsand other plant extracts. Journal of Applied Microbiology, 86, 985–990.

Hayouni, E. A., Chraief, I., Abedrabba, M., Bouix, M., Leveau, J. Y., Mohammed, H., et al.(2008). Tunisian Salvia officinalis L. and Schinus molle L. essential oils: Their chem-ical compositions and their preservative effects against Salmonella inoculated inminced beef meat. International Journal of Food Microbiology, 125, 242–251.

Helander, I. M., Alakomi, H. L., Latva-Kala, K., Mattila-Sandholm, T., Pol, I., Smid, E. J.,et al. (1998). Characterization of the action of selected essential oil componentson Gram-negative bacteria. Journal of Agricultural and Food Chemistry, 46(9),3590–3595.

Holley, R. A., & Patel, D. (2005). Improvement in shelf-life and safety of perishablefoods by plant essential oils and smoke antimicrobials. Food Microbiology, 22,273–292.

Humphrey, T., & Jorgensen, F. (2006). Review. Pathogens on meat infection in animalsestablishing a relationship using Campylobacter and Salmonella as examples. MeatScience, 74, 89–97.

Ilsley, S., Miller, H., Greathead, H., & Kamel, C. (2002). Herbal sow diets boost pre-weaning growth. Pig Progress, 18(4), 8–10.

Iseppi, R., Pilati, F., Marini, M., Toselli, M., de Niederhausern, S., Guerrieri, E. M., et al.(2008). Anti-listerial activity of a polymeric film coated with hybrid coatings dopedwith Enterocin 416K1 for use as bioactive food packaging. International Journal ofFood Microbiology, 123, 281–287.

Jamshidi, A., Bassami, M. R., & Afshari-Nic, S. (2008). Identification of Salmonella sppand Salmonella Typhimurium by multiplex PCR-based assay from poultry carcassesin Mashhad. Iranian International Journal of Veterinary Research, 3(1), 43–48.

Johny, A. K., Darre, M. J., Donoghue, A. M., Donoghue, D. J., & Venkitanarayanan, K.(2010). Antibacterial effect of trans-cinnamaldehyde, eugenol, carvacrol, and thy-mol on Salmonella Enteritidis and Campylobacter jejuni in chicken cecal contentsin vitro. Journal of Applied Poultry Research, 19, 237–244.

Juliano, C., Mattana, A., & Usai, M. (2000). Composition and in vitro antimicrobial activ-ity of the essential oil of Thymus herba-barona Loisel growing wild in Sardinia.Journal of Essential Oil Research, 12, 516–522.

Juven, B. J., Kanner, J., Schved, F., & Weisslowicz, H. (1994). Factors that interact withthe antibacterial action of thyme essential oil and its active constituents. The Journalof Applied Bacteriology, 76, 626–631.

Karabagias, I., Badeka, A., & Kontominas, M. G. (2011). Shelf life extension of lamb meatusing thyme or oregano essential oils and modified atmosphere packaging. MeatScience, 88, 109–116.

Karatzas, A. K., Kets, E. P. W., Smid, E. J., & Bennik, M. H. J. (2001). The combined actionof carvacrol and high hydrostatic pressure on Listeria monocytogenes Scott A. Journalof Applied Microbiology, 90, 463–469.

Kim, J., Marshall, M. R., Cornell, J. A., Preston, J. F., & Wei, C. I. (1995). Antibacterial ac-tivity of carvacrol, citral, and geraniol against Salmonella Typhimurium in culturemedium and on fish cubes. Journal of Food Science, 60, 1364–1374.

Kim, J., Marshall, M. R., & Wei, C. I. (1995). Antibacterial activity of some essential oilcomponents against five foodborne pathogens. Journal of Agricultural and FoodChemistry, 43, 2839–2845.

Knobloch, K., Pauli, A., Iberl, B., Weigand, H., & Weis, N. (1989). Antibacterial and anti-fungal properties of essential oil components. Journal of Essential Oil Research, 1,119–128.

Knobloch, K., Weigand, H., Weis, N., Schwarm, H. M., & Vigenschow, H. (1986). Actionof terpenoids on energy metabolism. In E. J. Brunke (Ed.), Progress in Essential OilResearch: 16th International Symposium on Essential Oils (pp. 429–445). Berlin: DeGruyter.

Koutsoumanis, K., Lambropoulou, K., & Nychas, G. J. F. (1999). A predictive model forthe non-thermal inactivation of Salmonella Enteritidis in a food model system sup-plemented with a natural antimicrobial. International Journal of Food Microbiology,49, 63–74.

Lambert, R. J. W., Skandamis, P. N., Coote, P., & Nychas, G. J. E. (2001). A study of theminimum inhibitory concentration and mode of action of oregano essential oil,thymol and carvacrol. Journal of Applied Microbiology, 91, 453–462.

Lee, K. W., Everts, H., Kappert, H. J., Yeom, K. H., & Beynen, A. C. (2003). Dietary carva-crol lowers body weight gain but improves feed conversion in female broilerchickens. Journal of Applied Poultry Research, 12, 394–399.

Leistner, L. (1978). Hurdle effect and energy saving. In W. K. Downey (Ed.), Food qualityand nutrition (pp. 553). London: Applied Science Publication.

Lopez, P., Sanchez, C., Batlle, R., & Nerın, C. (2007). Development of flexible antimicro-bial films using essential oils as active agents. Journal of Agricultural and FoodChemistry, 55, 8814–8824.

Lopez, P., Sanchez, C., Battle, R., & Nerin, C. (2005). Solid- and vapor-phase antimi-crobial activities of six essential oils: Susceptibility of selected foodborne bac-terial and fungal strains. Journal of Agricultural and Food Chemistry, 53,6939–6946.

Mahmoud, S. S., & Croteau, R. B. (2002). Strategies for transgenic manipulation ofmonoterpene biosynthesis in plants. Trends in Plant Science, 7(8), 366–373.

Marino, M., Bersani, C., & Comi, G. (2001). Impedance measurements to study the an-timicrobial activity of essential oils from Lamiaceace and Compositae. InternationalJournal of Food Microbiology, 67, 187–195.


Matan, N., Rimkeeree, H., Mawson, A. J., Chompreeda, P., Haruthaithanasan, V., Parker,M., et al. (2006). Antimicrobial activity of cinnamon and clove oils under modi-fied atmosphere conditions. International Journal of Food Microbiology, 107,180–185.

Mattson, T. E., Johny, A. K., Amalaradjou, M. A. R., More, K., Schreiber, D. T., Patel, J., et al.(2011). Inactivation of Salmonella spp. on tomatoes by plant molecules. Interna-tional Journal of Food Microbiology, 144, 464–468.

McCaskill, D., & Croteau, R. (1999). Strategies for bioengineering the development andmetabolism of glandular tissues in plants. Nature Biotechnology, 17, 31–36.

Mead, P. S., Slutsker, L., Detz, V., McCaig, L. F., Breese, J. S., Shapiro, C., et al. (1999). Foodrelated illness and dead in the United States. Emerging Infectious Diseases, 5,607–625.

Mejlholm, O., & Dalgaard, P. (2002). Antimicrobial effect of essential oils on the seafoodspoilage micro-organism Photobacterium phosphoreum in liquid media and fishproducts. Letters in Applied Microbiology, 34, 27–31.

Mendoza-Yepes, M. J., Sanchez-Hidalgo, L. E., Maertens, G., & Marin-Iniesta, F. (1997).Inhibition of Listeria monocytogenes and other bacteria by a plant essential oil(DMC) en Spanish soft cheese. Journal of Food Safety, 17, 47–55.

Miltz, J., Rydlo, T., Mor, A., & Polyakov, V. (2006). Potency evaluation of a dermaseptinS4 derivative for antimicrobial food packaging applications. Packaging Technologyand Science, 19, 345–354.

Min, S., Harris, L. J., Han, J. H., & Krochta, J. M. (2005). Listeria monocytogenes inhibitionby whey protein films and coatings incorporating lysozyme. Journal of Food Protec-tion, 68(11), 2317–2325.

Moleyar, V., & Narasimham, P. (1992). Antibacterial activity of essential oil compo-nents. International Journal of Food Microbiology, 16, 337–342.

Moosavy, M. H., Basti, A. A., Misaghi, A., Salehi, T. Z., Abbasifar, R., Ebrahimzadeh Mousavi,H. A., et al. (2008). Effect of Zatariamultiflora Boiss. essential oil andnisin on SalmonellaTyphimurium and Staphylococcus aureus in a food model system and on the bacterialcell membranes. Food Research International, 41, 1050–1057.

Mourey, A., & Canillac, N. (2002). Anti-Listeria monocytogenes activity of essential oilscomponents of conifers. Food Control, 13, 289–292.

Nychas, G. J. E. (1995). Natural antimicrobials from plants. In G. W. Gould (Ed.), Newmethods of food preservation (pp. 58–89). London: Blackie Academic andProfessional.

O'Brien, T. F. (2002). Emergence, spread, and environmental effect of antimicrobial re-sistance: How use of an antimicrobial anywhere can increase resistance to any an-timicrobial anywhere else. Clinical Infectious Diseases, 34, 78–84.

Oosterhaven, K., Poolman, B., & Smid, E. J. (1995). S-carvone as a natural potato sproutinhibiting, fungistatic and bacteristatic compound. Industrial Crops and Products, 4,23–31.

Ordonez, G., Llopis, N., & Penalver, P. (2008). Efficacy of eugenol against a Salmonellaenterica serovar Enteritidis experimental infection in commercial layers in produc-tion. Journal of Applied Poultry Research, 17, 376–382.

Oussalah, M., Caillet, S., & Lacroix, M. (2006). Mechanism of action of Spanish oregano,Chinese cinnamon, and savory oils against cell membrane and walls of Escherichiacoli O157:H7 and Listeria monocytogenes. Journal of Food Protection, 69(5),1046–1055.

Oussalah, M., Caillet, S., Sauciere, L., & Lacroix, M. (2007). Inhibitory effects of selectedplant essential oils on the growth of four pathogenic bacteria: E. coli O157:H7, Sal-monella Typhimurium, Staphylococcus aureus and Listeria monocytogenes. FoodControl, 18(5), 414–420.

Oussallah, M., Caillet, S., Salmieri, S., Saucier, L., & Lacroix, M. (2004). Antimicrobial andantioxidant effects of milk protein based film containing essential oils for the pres-ervation of whole beef muscle. Journal of Agriculture and Food Chemistry, 52,5598–5605.

Pandit, V. A., & Shelef, L. A. (1994). Sensitivity of Listeria monocytogenes to rosemary(Rosmarinus officinalis L.). Food Microbiology, 11, 57–63.

Paranagama, P. A., Abeysekera, K. H. T., Abeywickrama, K., & Nugaliyadd, L. (2003).Fungicidal and anti-aflatoxigenic effects of the essential oil of Cymbopogon citratus(DC.) Stapf. (lemongrass) against Aspergillus flavus Link isolated from stored rice.Letters in Applied Microbiology, 37, 86–90.

Parish, E. P., Baum, D., Kryger, R., Goodrich, R., & Baum, R. (2003). Fate of Salmonellae incitrus oils and aqueous aroma. Journal of Food Protection, 66(9), 1704–1707.

Paster, N., Menasherov, M., Ravid, U., & Juven, B. (1995). Antifungal activity of oreganoand thyme essential oils applied as fumigants against fungi attacking stored grain.Journal of Food Protection, 58, 81–85.

Pichersky, E., Noel, J. P., & Dudareva, N. (2006). Biosynthesis of plant volatiles: Nature'sdiversity and ingenuity. Science, 311, 808–811.

Plackett, D., & Ghambari-Siahkali, A. L. (2007). Behaviour of alpha and beta-cyclodextrin-encapsulated allyl isothiocyanate as slow release additives inpolylactide-co-polycaprolactone films. Journal of Applied Polymer Science, 105,2850–2857.

Pol, I. E., Mastwijk, H. C., Slump, R. A., Popa, M. E., & Smid, E. J. (2001). Influence of foodmatrix on inactivation of Bacillus cereus by combinations of nisin, pulsed electricfield treatment and carvacrol. Journal of Food Protection, 64(7), 1012–1018.

Quintavalla, S., & Vicini, L. (2002). Antimicrobial food packaging in meat industry.MeatScience, 62, 373–380.

Rabsch, W., Tschäpe, H., Andreas, J., & Bäumler, A. J. (2001). Review, non-typhoidal sal-monellosis: Emerging problems. Microbes and Infection, 3, 237–247.

Rahman, A., Al-Reza, S. M., Yoon, J. I., & Kang, S. C. (2009). In vitro inhibition of food-borne pathogens by volatile oil and organic extracts of Poncirus trifoliata Rafin.seeds. Journal of the Science of Food and Agriculture, 89, 876–881.

Rahman, M. U., Gul, S., & Dhano, E. A. (2008). Antimicrobial activities of Ferula assafoetidaoil against Gram positive and Gram negative bacteria. American–Eurasian Journal ofAgricultural and Environmental Science, 4(2), 203–206.

Rahman, A., Lee, J. G., & Kang, S. C. (2009). In vitro control of food-borne and food spoil-age bacteria by essential oil and ethanol extracts of Lonicera japonica Thunb. FoodChemistry, 116, 670–675.

Rasooli, I., Rezaei, M. B., & Allameh, A. (2006). Ultrastructural studies on antimicrobialefficacy of thyme essential oils on Listeria monocytogenes. International Journal ofInfectious Diseases, 10(3), 236–241.

Rattanachaikunsopon, P., & Phumkhachorn, P. (2010). Antimicrobial activity of basil(Ocimum basilicum) oil against Salmonella Enteritidis in vitro and in food. Bioscience,Biotechnology, and Biochemistry, 74(6), 1200–1204.

Ravishankar, S., Zhu, L., Olsen, C. W., McHugh, T. H., & Friedman, M. (2009). Edibleapple film wraps containing plant antimicrobials inactivate foodborne pathogenson meat and poultry products. Journal of Food Science, 74, 440–445.

Ravishankar, S., Zhu, L., Reyna-Granados, J., Law, B., Joens, L., Friedman, M., et al. (2010).Carvacrol and cinnamaldehyde inactivate antibiotic-resistant Salmonella Entericain buffer and on celery and oysters. Journal of Food Protection, 73(2), 234–240.

Raybaudi-Massilia, R. M., Mosqueda-Melgar, J., & Martín-Belloso, O. (2006). Antimicro-bial activity of essential oils on Salmonella Enteritidis, Escherichia coli, and Listeriainnocua in fruit Juices. Journal of Food Protection, 69, 1579–1586.

Rees, C. E. D., Dodd, C. E. R., Gibson, P. T., Booth, I. R., & Stewart, G. S. A. B. (1995).The significance of bacteria in stationary phase to food microbiology. InternationalJournal of Food Microbiology, 28, 263–275.

Rodriguez, A., Nerın, C., & Batlle, R. (2008). New cinnamon-based active paper packagingagainst Rhizopus stolonifer food spoilage. Journal of Agricultural and Food Chemistry, 56,6364–6369.

Roldán, L. P., Díaz, G. J., & Duringer, J. M. (2010). Composition and antibacterial activityof essential oils obtained from plants of the Lamiaceae family against pathogenicand beneficial bacteria. Revista Colombiana de Ciencias Pecuarias, 23(4) (pp.).

Roller, S., & Seedhar, P. (2002). Carvacrol and cinnamic acid inhibit microbial growth infresh-cut melon and kiwifruit at 4 °C and 8 °C. Letters in Applied Microbiology, 35,390–394.

Rude, R. A., Jackson, G. L., Bier, J. W., Sawyer, T. K., & Risty, N. G. (1984). Survey of freshvegetables for nematodes, amoebae and Salmonella. Journal of the Association ofOfficial Analytical Chemists, 67, 613–615.

Salgueiro, L. R., Vila, R., Tomi, F., Figueiredo, A. C., Barroso, J. G., Canigueral, S., et al.(1997). Variability of essential oils of Thymus caespititius from Portugal. Phyto-chemistry, 45, 307–311.

Seydim, A. C., & Sarikus, G. (2006). Antimicrobial activity of whey protein based ediblefilms incorporated with oregano, rosemary and garlic essential oils. Food ResearchInternational, 39, 639–644.

Shelef, L. A. (1983). Antimicrobial effects of spices. Journal of Food Safety, 6, 29–44.Shelef, L. A., Jyothi, E. K., & Bulgarelli, M. A. (1984). Growth of enteropathogenic and

spoilage bacteria in sage-containing broth and foods. Journal of Food Science, 49,737–740.

Shin, S. W. (2005). In vitro effects of essential oils from Ostericum koreanum againstantibiotic-resistant Salmonella spp. Archives of Pharmacal Research, 28(7), 765–769.

Shin, S. W. (2005). Anti-Salmonella activity of lemongrass oil alone and in combinationwith antibiotics. Natural Products Science, 11(3), 160–164.

Sikkema, J., De Bont, J. A. M., & Poolman, B. (1995). Mechanisms of membrane toxicityof hydrocarbons. Microbiological Reviews, 59(2), 201–222.

Singh, N., Singh, R. K., Bhunia, A. K., & Stroshine, R. L. (2002). Efficacy of chlorine diox-ide, ozone and thyme essential oil or a sequential washing in killing Escherichia coliO157:H7 on lettuce and baby carrots. Lebensmittelwissenchaften und Technologien,35, 720–729.

Skandamis, P. N., & Nychas, G. J. E. (2000). Development and evaluation of a model pre-dicting the survival of Escherichia coli O157:H7 NCTC 12900 in homemade eggplantsalad at various temperatures, pHs and oregano essential oil concentrations. Appliedand Environmental Microbiology, 66(4), 1646–1653.

Skandamis, P. N., & Nychas, G. J. E. (2001). Effect of oregano essential oil on microbio-logical and physico-chemical attributes of minced meat stored in air and modifiedatmospheres. Journal of Applied Microbiology, 91, 1011–1022.

Skandamis, P., Tsigarida, E., & Nychas, G. J. E. (2000). Ecophysiological attributes of Sal-monella Typhimurium in liquid culture and within a gelatin gel with or without theaddition of oregano essential oil. World Journal of Microbiology and Biotechnology,16, 31–35.

Smid, E. J., & Gorris, L. G. M. (1999). Natural antimicrobials for food preservation. In M. S.Rahman (Ed.),Handbook of Food Preservation (pp. 285–308). NewYork:Marcel Dekker.

Smith-Palmer, A., Stewart, J., & Fyfe, L. (2001). The potential application of plant essen-tial oils as natural food preservatives in soft cheese. Food Microbiology, 18,463–470.

Smits, C. H. M., Veldman, A., Verstegen, M. W. A., & Beynen, A. C. (1997). Dietary car-boxylmethylcellulose with high instead of low viscosity reduces macronutrientdigestion in broiler chickens. The Journal of Nutrition, 127, 483–487.

Smoley, C. K. (1993). U.S. Food and Drug Administration. Everything Added to Food inthe United States. Boca Raton, FL: CRC Press, Inc..

Sridhar, S. R., Rajagopal, R. V., Rajavel, R., Masilamani, S., & Narsimhan, S. (2003). Anti-fungal activities of some essential oils. Journal of Agricultural and Food Chemistry,51, 7596–7599.

Stecchini, M. L., Sarais, I., & Giavedoni, P. (1993). Effect of essential oils on Aeromonashydrophila in a culture medium and in cooked pork. Journal of Food Protection,56(5), 406–409.

Suppakul, P., Miltz, J., Sonneveld, K., & Bigger, S. W. (2006). Characterization of antimi-crobial films containing basil extracts. Packaging Technology and Science, 19,259–268.

Tassou, C., Drosinos, E. H., & Nychas, G. J. E. (1995). Effects of essential oil from mint(Mentha piperita) on Salmonella Enteritidis and Listeria monocytogenes in modelfood systems at 4 °C and 10 °C. The Journal of Applied Bacteriology, 78, 593–600.


Tassou, C., Drosinos, E. H., & Nychas, G. J. E. (1996). Inhibition of resident microbial floraand pathogen inocula on cold fresh fish fillets in olive oil, oregano, and lemon juiceunder modified atmosphere or air. Journal of Food Protection, 59(1), 31–34.

Tharanathan, R. N. (2003). Biodegradable films and composite coatings: Past, presentand future. Trends in Food Science and Technology, 14, 71–78.

Tsigarida, E., Skandamis, P., & Nychas, G. J. E. (2000). Behaviour of Listeria monocyto-genes and autochthonous flora on meat stored under aerobic, vacuum and modi-fied atmosphere packaging conditions with or without the presence of oreganoessential oil at 5 °C. Journal of Applied Microbiology, 89, 901–909.

Tuley de Silva, K. (1996). A manual on the essential oil industry. (Ed.), United NationsIndustrial Development Organization, Vienna.

Turgis, M., Han, J., Borsa, J., & Lacroix, M. (2008). Combined effect of natural essentialoils, modified atmosphere packaging, and gamma radiation on the microbialgrowth on ground beef. Journal of Food Protection, 71(6), 1237–1243.

Ultee, A., Slump, R. A., Steging, G., & Smid, E. J. (2000). Antimicrobial activity of carva-crol toward Bacillus cereus on rice. Journal of Food Protection, 63(5), 620–624.

Ultee, A., & Smid, E. J. (2001). Influence of carvacrol on growth and toxin production byBacillus cereus. International Journal of Food Microbiology, 64, 373–378.

Valverde, M. T., Iniesta, F. M., Garrido, L. C., Rodríguez, A. T., García-García, I., Macanas,H., et al. (2010). Inactivation of Salmonella spp in refrigerated liquid egg productsusing essential oils and their active compounds. Proceedings in International Confer-ence on Food Innovation “Food Innova”, Universitydad Politecnica De Valencia.

Van de Braak, S. A. A. J., & Leijten, G. C. J. J. (1999). Essential oils and oleoresins: A survey inthe Netherlands and other major markets in the European Union (pp. 116). Rotterdam:CBI, Centre for the Promotion of Imports from Developing Countries.

Van Krimpen, M. M., & Binnendijk, G. P. (2001). RopadiarR as alternative for antimicro-bial growth promoter in diets of weanling pigs (pp. 14). Lelystad: PraktijkonderzoekVeehouderij.

VanWelie, R. T. H. (1997).Alle cosmetica ingredie¨nten en hun functies (pp. 126).Nieuwegein:Nederlandse Cosmetica Vereniging.

Veldman, A., & Enting, H. (1996). Effects of crina HC 737 in feed on broiler performanceand digestive physiology and microbiology. CLO-institute for Animal Nutrition “DeSchothorst”.

Venskutonis, P. R. (1996). Effect of drying on the volatile constituents of thyme (Thymusvulgaris L.) and sage (Salvia officinalis L.). Food Chemistry, 2, 219–227.

Vermeiren, L., Devlieghere, F., van Beest, M., de Kruiif, N., & Debevere, J. (1999). Devel-opments in the active packing of foods. Trends in Food Science and Technology, 10,77–86.

Wan, J., Wilcock, A., & Coventry, M. J. (1998). The effect of essential oils of basil on thegrowth of Aeromonas hydrophila and Pseudomonas fluorescens. Journal of AppliedMicrobiology, 84, 152–158.

Weissinger, W. R., McWatters, K. H., & Beuchat, L. R. (2001). Evaluation of volatilechemical treatments for lethality to Salmonella on alfalfa seeds and sprouts. Journalof Food Protection, 64(4), 442–450.

Wells, J. M., & Butterfield, J. E. (1997). Salmonella contamination associated with bacte-rial soft rot of fresh fruits and vegetables in the marketplace. Plant Diseases, 81,867–872.

Wendakoon, C. N., & Sakaguchi, M. (1993). Combined effect of sodium chloride andclove on growth and biogenic amine formation of Enterobacter aerogenes in mack-erel muscle extract. Journal of Food Protection, 56(5), 410–413.

Wendakoon, C. N., & Sakaguchi, M. (1995). Inhibition of amino acid decarboxylaseactivity of Enterobacter aerogenes by active components in spices. Journal of FoodProtection, 58(3), 280–283.

WHO (2002). Food safety and foodborne illness. World Health Organization Fact sheet237, revised January 2002. Geneva.

WHO (2002). World health report 2002: Reducing risks, promoting healthy life. Geneva:World Health Organization (30 October 2002).

Williams, P., & Losa, R. (2001). The use of essential oils and their compounds in poultrynutrition. World Poultry, 17, 14–15.

Yoon, J. I., Bajpai, V. K., & Kang, S. C. (2011). Synergistic effect of nisin and cone essentialoil of Metasequoia glyptostroboides Miki ex Hu against Listeria monocytogenes inmilk samples. Food and Chemical Toxicology, 49(1), 109–114.

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