antiamoeba

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M.Ma Food Mb Food SCA 956

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. . . . . .icrobiaals. . . .ent inls . . . . .. . . . . .ic effecto exper. . . . . .

6.2. Fish. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12116.3. Dairy products . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12116.4. Vegetables . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12116.5. Rice. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12116.6. Fruit . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12116.7. Animal feed . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1212

* Corresponding author. Tel.: +1 (336)334 7933; fax: +1 (336)334 7239.

Food Control 21 (2010) 11991218

Contents lists available at ScienceDirectE-mail address: [email protected] (M.M. Tajkarimi).5.2. Bacillus sp. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12045.3. C. jejuni . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12065.4. Clostridium perfringens . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12085.5. Escherichia coli . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12085.6. L. monocytogenes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12085.7. Molds and yeasts. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12085.8. Pseudomonas sp. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12095.9. Salmonella sp. and Shigella sp. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12095.10. Staphylococcus aureus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12095.11. Vibrio parahaemolyticus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12095.12. General Gram-positive and Gram-negative bacteria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1209

6. Some in-food experiments with plant-origin antimicrobials. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12106.1. Meat and poultry products . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1210Contents

1. Introduction . . . . . . . . . . . . . . . . .2. Historical overview of plant antim3. Major spice and herb antimicrobi

3.1. Chemical components pres4. Uses of plant-origin antimicrobia

4.1. Mechanism of action. . . . .4.2. Synergistic and antagonist

5. Review of some findings of in vitr5.1. A. hydrophila . . . . . . . . . . .0956-7135/$ - see front matter 2010 Elsevier Ltd. Adoi:10.1016/j.foodcont.2010.02.003. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1200ls . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1201. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1201EOs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1201. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1202. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1203s of components . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1203iments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1204. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1204Food-borne pathogenseywords:erbs and spicesatural preservatives

applied in several in-food and in vitro experiments. This paper aims to review recent in-food applicationsof EOs and plant-origin natural antimicrobials and recent techniques for screening such compounds.

2010 Elsevier Ltd. All rights reserved.about their effects in food, strong odor, and high cost. Combinations of techniques have been successfullyccepted 2 February 2010 microbial effects comparable to synthetic additives is still remote for three major reasons: limited datad 9 December 2009d in revised form 27 January 2010

against pathogens, such as Salmonella typhimurium, Escherichia coli O157:H7, Listeria monocytogenes,Bacillus cereus and Staphylococcus aureus, in food systems. Application of herbs, spices and EOs with anti-rticle history:eceive

Herbs and spices containing essential oils (EOs) in the range of 0.050.1% have demonstrated activityimicrobial herb and spice compounds in food

. Tajkarimi a,*, S.A. Ibrahim a, D.O. Cliver b

icrobiology and Biotechnology Laboratory, North Carolina A&T State University, 171-B Carver Hall, Greensboro, NC 27411-1064, USAafety Laboratory, Department of Population Health and Reproduction, School of Veterinary Medicine, University of California, Davis One Shields Avenue, Davis,16-8743, USA

i c l e i n f o a b s t r a c teviewFood Control

journal homepage: www.elsevier .com/locate / foodcontll rights reserved.

. . .. . .. . .. . .. . .. . .. . .

Ryan, & Bourke, 2008b; Lopez-Malo vigil et al., 2005; Moriera,

uthprima2008;menta2&Ch

cinnamon and clove EOs to apple cider signicantly reduced the

of citric acid or up to 0.1% of cinnamon bark oil in tomato juice, fol-

Con008; Lopez-Malo vigil et al., 2005; Martinez, Obeso, Rodriguez, published mostly in the past 10 years on plant-derived compounds

Garailleasiyais a growing effort to develop new effective methods that relyrily on their use to enhance food safety (Ayala-Zavala et al.,Brandi et al., 2006; Chen et al., 2008; FAO/WHO Codex Ali-rius Commission., 2007; Liu, OConner, Cotter, Hill & Ross,

cessfully achieved the pasteurization level (reduction of at least 5.0log10 units) (Mosqueda-Melgar, Raybaudi-Massilia, & Martin-Bel-loso, 2008a, 2008b).

The purpose of this paper is to provide an overview of the datanderstanding of how natural antimicrobial substances work,ere

lowed by treatment with high-intensity pulsed electric elds, suc-et al., 2006; Ponce et al., 2008; Raybaudi, Mosqueda-Melgaret al., 2008; Zaika, 1988). Even without a more comprehensivePonce, Del Valle, & Roura, 2007; Patrignani et al., 2008; Periago D-value and time to 5-log reduction of Escherichia coli O157:H7(Knight & McKellar, 2007). Application of concentrations of 2.0%7. Effectiveness determinations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .7.1. Disc-diffusion method. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .7.2. Drop-agar-diffusion method . . . . . . . . . . . . . . . . . . . . . . . . . . .7.3. Broth microdilution method. . . . . . . . . . . . . . . . . . . . . . . . . . .7.4. Direct-contact technique in agar . . . . . . . . . . . . . . . . . . . . . . .

8. Conclusions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

1. Introduction

Strong consumer demand for safe and high-quality foods can beattributed in part to the widespread availability and accessibility ofquality health data and information. There are also new concernsabout food safety due to increasing occurrence of new food-bornedisease outbreaks caused by pathogenic micro-organisms. Thisraises considerable challenges, particularly since there is increas-ing unease regarding the use of chemical preservatives and arti-cial antimicrobials to inactivate or inhibit growth of spoilage andpathogenic micro-organisms (Arques, Rodriguez, Nunez, & Medina,2008; Aslim & Yucel, 2007; Brandi, Amagliani, Schiavano, De Santi,& Sisti, 2006; Cushnie & Lamb, 2005; Demirci, Guven, Demirci,Dadandi, & Baser, 2008; Friedman, Henika, Levin, & Mandrell,2006; Ionnouy, Poiata, Hancianu, & Tzakou, 2007; Li, Tajkarimi, &Osburn, 2008; Lopez-Malo vigil, Palou, & Alzamora, 2005; Murdak,Cleveland, Matthews, & Chikindas, 2007; Nguefack et al., 2007;Petitclerc et al., 2007; Turner, Thompson, & Auldist, 2007). As aconsequence, natural antimicrobials are receiving a good deal ofattention for a number of micro-organism-control issues. Reducingthe need for antibiotics, controlling microbial contamination infood, improving shelf-life extension technologies to eliminateundesirable pathogens and/or delay microbial spoilage, decreasingthe development of antibiotic resistance by pathogenic micro-organisms or strengthening immune cells in humans are some ofthe benets (Abou-taleb & Kawai, 2008; Fisher & Phillips, 2008;Gaysinsky & Weiss, 2007; Gutierrez, Barry-Ryan, & Bourke,2008a; Lopez-Malo vigil et al., 2005; Nazef, Belguesmia, Tani, Pre-vost, & Drider, 2008; Patrignani et al., 2008; Periago, Conesa, Del-gado, Fernndez, & Palop, 2006; Ponce, Roura, Del Valle, &Moreira, 2008; Raybaudi, Mosqueda-Melgar, & Martin-Belloso,2008;Yamamoto, Matsunaga, & Friedman, 2004).

Antimicrobials are used in food for two main reasons: (1) tocontrol natural spoilage processes (food preservation), and (2) toprevent/control growth of micro-organisms, including pathogenicmicro-organisms (food safety). Natural antimicrobials are derivedfrom animal, plant and microbial sources. There is considerable po-tential for utilization of natural antimicrobials in food, especially infresh fruits and vegetables. However, methods and mechanisms ofaction, as well as the toxicological and sensory effects of naturalantimicrobials, are not completely understood (Burt, 2004; David-son, 2006; Gaysinsky & Weiss, 2007; Gutierrez, Rodriguez, Barry-

1200 M.M. Tajkarimi et al. / Foodcia, 2008; Murdak et al., 2007; Nazef et al., 2008; Oussalah,t, Salmiea, Saucier, & Lacroix, 2004; Pellegrini, 2003; Vaga-& Chanda, 2007).. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1212. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1214. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1214. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1214. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1214. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1214. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1215

In addition to their avoring effects, some spices and herbshave antimicrobial effects on plant and human pathogens(Brandi et al., 2006). Food processing technologies such as chem-ical preservatives cannot eliminate food pathogens such as Liste-ria monocytogenesis or delay microbial spoilage totally (Gutierrez,Barry-Ryan, & Bourke, 2009). Cold distribution of perishable foodcan help, but it cannot guarantee the overall safety and qualityof the product. Moreover, changes in dietary habits and foodprocessing practices and increasing demand for ready-to-eatproducts. Fruits and vegetables have been followed byincreasing reports of food-borne pathogenic micro-organisms be-cause of the presence of pathogens in raw materials (Lanciottiet al., 2004; Li, Tajkarimi, & Osburn, 2008; Li, Zhu et al.,2008).

There are new techniques such as pulsed light, high pressurepulsed electric and magnetic elds for food preservation and con-trolling pathogens and spoilage micro-organisms in food. How-ever, technologies such as mild heat processing, modied-atmosphere packaging, vacuum packaging and refrigeration arenot sufciently effective, neither for eliminating undesirablepathogens nor delaying microbial spoilage. Moreover, some ofthese methods, such as vacuum cooling, can increase the proba-bility of food contamination. Incorporation of natural antimicro-bials into packaging materials, to protect the food surfacerather than the food, has also been developed recently (Abou-ta-leb & Kawai, 2008; Fisher & Phillips, 2008; Gaysinsky & Weiss,2007; Gutierrez et al., 2008a; Holley & Patel, 2005; Lanciottiet al., 2004; Li, Tajkarimi et al., 2008; Li, Zhu et al., 2008; Lo-pez-Malo vigil et al., 2005; Nazef et al., 2008; Patrignani et al.,2008; Periago et al., 2006; Ponce et al., 2008; Raybaudi, Mosque-da-Melgar et al., 2008; Raybaudi, Rojas-Grau, Mosqueda-Melgar,& Martin-Belloso, 2008). A growing body of data indicates thatthere is considerable potential for utilization of natural antimi-crobials in food, especially application to fresh fruits and vegeta-bles, for their oxidative degradation of lipids and improvement ofthe quality and nutritional value of food, in addition to theirstrong antifungal effects. EOs derived from spices and plants haveantimicrobial activity against L. monocytogenes, Salmonellatyphimurium, Escherichia coli O157:H7, Shigella dysenteriae, Bacil-lus cereus and Staphylococcus aureus at levels between 0.2 and10 ll ml1(Burt, 2004).

For example, combined mild heat treatment with addition of

trol 21 (2010) 11991218that have been reported to be effective against spoilage or patho-genic bacteria, and practical methods for screening thesecompounds.

Negi, Jena, & Jagan Mohan Rao, 2007; Kwon, Kwon, Kwon, & Lee,2008; Soa, Prasad, Vijay, & Srivastava, 2007; Zaika, 1988).

ConMost spices have eastern origins; however, some of them havebeen introduced after discovery of the New World spices such aschili peppers, sweet peppers, allspice, annatto, chocolate, epazote,sassafras, and vanilla, which have been used for food avoring andmedicinal purposes (Ceylan & Fung, 2004).

3. Major spice and herb antimicrobials

Spices and EOs are used by the food industry as natural agents forextending the shelf life of foods. A variety of plant- and spice-basedantimicrobials is used for reducing or eliminating pathogenic bacte-ria, and increasing the overall quality of food products. Plant-originantimicrobials are obtained by various methods from aromatic andvolatile oily liquids from owers, buds, seeds, leaves, twigs, bark,herbs, wood, fruits and roots of plants. EOs in plants generally aremixtures of several components. Some of those presence exert anti-microbial effects such as components in oregano, clove, cinnamon,citral, garlic, coriander, rosemary, parsley, lemongrass, sageandvan-illin (Angioni et al., 2004; Arques et al., 2008;Daferera, Ziogas, & Pol-issiou, 2000; Davidson&Naidu, 2000; Gutierrez et al., 2008a; Holley& Patel, 2005; Kim, Kubec, & Musah, 2006; Kim, Wei, & Marshall,1995; Lopes-Lutz, Alviano, Alviano, & Kolodziejczyk, 2008; Naidu,2000a; Periago et al., 2006; Proestos, Boziaris, Kapsokefalou, &Komaitis, 2008; Santos & Rao, 2001; Silva et al., 2007; Skocibusic,Bezic,&Dunkic, 2006;Yoshidaet al., 1999).Other spices, suchas gin-ger, blackpepper, redpepper, chili powder, cuminandcurrypowder,showed lower antimicrobial properties (Holley & Patel, 2005).

There are more than 1340 plants with dened antimicrobialcompounds, and over 30,000 components have been isolated fromphenol group-containing plant-oil compounds and used in the foodindustry. However, commercially useful characterizations of pre-servative properties are available for only a few EOs. There is a needfor more evaluation of EOs in eld and food systems. Food-preser-2. Historical overview of plant antimicrobials

Natural antimicrobial agents derived from sources such as plantoils have been recognized and used for centuries in food preserva-tion. EOs and spiceswere used by the early Egyptians and have beenused for centuries inAsiancountries suchasChinaand India. Someofthe spices, such as clove, cinnamon,mustard, garlic, ginger andmintare still applied as alternative health remedies in India. EO produc-tion can be traced back over 2000 years to the Far East, with thebeginnings of more modern technologies occurring in Arabia in the9th century. However, it was also during this time period that themedical applications of EOs became secondary to their use for avorand aroma. Plant extracts and spices, in addition to contributing totaste and avor, can act against Gram-positive pathogens such asL. monocytogenes. They can also enhance storage stability by meansof active components including phenols, alcohols, aldehydes, ke-tones, ethers and hydrocarbons, especially in such spices as cinna-mon, clove, garlic, mustard, and onion. The rst scientic studiesof the preservation potential of spices, describing antimicrobialactivity of cinnamon oil against spores of anthrax bacilli, were re-ported in the 1880s. Moreover, clove was used as a preservative todisguise spoilage in meat, syrups, sauces and sweetmeats. In the1910s, cinnamon and mustard were shown to be effective in pre-serving applesauce. Since thenother spices, such as allspice, bay leaf,caraway, coriander, cumin, oregano, rosemary, sageand thyme,havebeen reported to have signicant bacteriostatic properties (Burt,2004; Ceylan & Fung, 2004; Gutierrez et al., 2008a; Jayaprakasha,

M.M. Tajkarimi et al. / Foodvative utilization of spices and their EOs as natural agents has re-cently been focused on extending the shelf life of foods, reducingor eliminating pathogenic bacteria, and increasing overall qualityof food products (Burt, 2004; Davidson, 2006; Gaysinsky & Weiss,2007; Gutierrez et al., 2008a; Lopez-Malo vigil et al., 2005; Morieraet al., 2007; Patrignani et al., 2008; Periago et al., 2006; Ponce et al.,2008; Raybaudi, Rojas-Grau et al., 2008; Razzaghi-Abyaneh et al.,2008; Zaika, 1988). Commercially based plant-origin antimicrobialsare most commonly produced by SD (steam distillation) and HD(hydro distillation) methods, and alternative methods such as SFE(supercritical uid extraction) provide higher solubility and im-proved mass transfer rates. Moreover, the manipulation of param-eters such as temperature and pressure leads to the extraction ofdifferent components when a particular component is required.Bioengineering of the EO components also provides more availablecommercial products (Burt, 2004). Edible, medicinal and herbalplants and spices such as oregano, rosemary, thyme, sage, basil, tur-meric, ginger, garlic, nutmeg, clove, mace, savory, and fennel, havebeen successfully used alone or in combination with other preser-vationmethods. They exert direct or indirect effects to extend food-stuff shelf life or as antimicrobial agent against a variety of Gram-positive and Gram-negative bacteria However, their efcacy de-pends on the pH, the storage temperature, the amount of oxygen,the EO concentration and active components (Burt et al., 2007;Du & Li, 2005; Gutierrez et al., 2008a; Holley & Patel, 2005; Kout-soumanis, Lambropoulou, & Nychas, 1999; Sandasi, Leonard, & Vil-joen, 2008; Svoboda, Brooker, & Zrustova, 2006; Viuda-Martos,Ruiz-Navajas, Fernandez-Lopez, & Angel Perez-Alvarez, 2008).

3.1. Chemical components present in EOs

EOs are a group of terpenoids, sesquiterpenes and possiblyditerpenes with different groups of aliphatic hydrocarbons, acids,alcohols, aldehydes, acyclic esters or lactones (Fisher & Phillips,2006). EOs and other plant extracts are principally responsiblefor antimicrobial activities in plants, herbs and spices. These ex-tracts can be obtained from plants and spices by various methods,such as steam, cold, dry and vacuum distillation. These plant com-pounds, including glucosides, saponins, tannins, alkaloids, EOs, or-ganic acids and others, are present as parts of the original plantdefense system against microbial infection (Bajpai, Rahman, &Kang, 2008; Ceylan & Fung, 2004). Major components of the EOscan constitute up to 85%, and other components are usually attrace levels (Burt, 2004; Grosso et al., 2008).

There are various chemical components present in plant-originantimicrobials including, saponin and avonoids, thiosulnates,glucosinolates and saponins.

Saponin and avonoids are found in fruits, vegetables, nuts,seeds, stems, owers, tea, wine, propolis and honey. They com-monly form a soapy lather after shaking in water. The antimicro-bial activity of saponins and avonoids in plants like oats (Avenasativa) and anthraquinones, carbohydrates and alkaloids derivedfrom plants like Bersama engleriana (Melianthaceae) have beenproven when extracted from roots, stem bark, leaves and wood(Bahraminejad, Asenstorfer, Riley, & Schultz, 2008; Cushnie &Lamb, 2005; Kuete et al., 2008; Musyimi, Muema, & Muema,2008; Naidu, 2000a). Thiosulnates are prepared from garlic bymild procedures. They have strong antimicrobial activities againstGram-negative bacteria (Kim et al., 2008; Naidu, 2000a; Yoshidaet al., 1999). Glucosinolates are present in broccoli, brussels sprouts,cabbage, and mustard powder and cause the pungent avor ofmustard and horseradish. They demonstrate a wide range of anti-bacterial and antifungal properties with direct or synergistic effectin combination with other compounds (Almajano, Carbo, LopezJimenez, & Gordon, 2008; Graumann & Holley, 2008; Gutierrezet al., 2008a; Naidu, 2000a; Tolonen et al., 2004). Generally,

trol 21 (2010) 11991218 1201phenolic compounds of EOs such as citrus oils extracted fromlemon, olive oil (oleuropein) and tea-tree oil (terpenoids), orangeand bergamot have broader antimicrobial effects and are not cate-

gorized as spices. Meanwhile, there are increasing reports of non-phenolic compounds of oils, which are effective against bothGram-positive and Gram-negative groups, from oregano, clove,cinnamon, citral, garlic, coriander, rosemary, parsley, lemongrass,purple (cultivar Ison) and bronze (cultivar Carlos) muscadine seedsand sage (Angioni et al., 2004; Daferera et al., 2000; Davidson &Naidu, 2000; El-Seedi et al., 2008; Fisher & Phillips, 2006; Gutierrezet al., 2008a; Holley & Patel, 2005; Kim, Marshall, Cornell, Preston,& Wei, 1995; Kim et al., 2008; Lopes-Lutz et al., 2008; Naidu,2000b; Nejad Ebrahimi, Hadian, Mirjalili, Sonboli, & Yousefzadi,2008; Mandalari et al., 2007; Nguefack et al., 2007; Oussalahet al., 2004; Santos & Rao, 2001; Skocibusic et al., 2006; Yoshidaet al., 1999).

4. Uses of plant-origin antimicrobials

genic and spoilage micro-organisms. Hydro-distilled EOs isolatedfrom the oral parts of Nandina domestica Thunb showed potentialactivity against food-borne pathogenic and spoilage bacteria (Bajpaiet al., 2008). Oregano, savory and thyme, which have terpenes, car-vacrol, p-cymene, and thymol, have demonstrated antifungal andantimicrobial activity that has attracted attention recently becauseof their potential food safety applications, especially for oregano(Bendahou et al., 2008; Naidu, 2000b).

Olive leaves (Olea europaea) showed antimicrobial effectsagainst Campylobacter jejuni, Helicobacter pylori and Staphylococcusaureus (Sudjana et al., 2009). Ethanolic leaf extract of Lonicera japon-ica Thunb showed antimicrobial effects against some food-bornepathogens and potential use for food processing (Rahman & Kang,2009). Thymus pallescent from different harvest locations showeddifferent antimicrobial activities (Hazzit, Baaliouamer, Verissimo,Falerio, & Miguel, 2009). However, location has not shown a differ-

Ad

rs

1202 M.M. Tajkarimi et al. / Food Control 21 (2010) 11991218Food spoilage can occur from raw food materials to the process-ing and distribution. Spoilage sources might be chemical, physicaland microbiological. Preservation techniques for microbiologicalspoilage have been dramatically improved in recent years tominimize any growth of micro-organisms including pathogenic mi-cro-organisms (Gould, 1996). Research concerning plant-originfood-preservative EOs has increased since the 1990s, withmore uti-lization of spices and their EOs as natural bio-preservatives, to in-crease shelf life and overall quality of food products and reduce oreliminate pathogenic micro-organisms (Burt, 2004; Moriera et al.,2007; Simitzis et al., 2008). Application of Thymus eigii showedstronger antimicrobial activity compared to vancomycin (30 mcg)and erythromycin (15 mcg) (Toroglu, 2007). Ginger (Zingiber ofci-nale), galangal (Alpinia galanga), turmeric (Curcuma longa), and n-gerroot (Boesenbergia pandurata) extracts against Gram-positiveand Gram-negative pathogenic bacteria at 0.20.4% (v/v) for nger-root and 810% (v/v) for all of the spices (Pattaratanawadee, Thong-son, Mahakarnchanakul, & Wanchaitanawong, 2006). Cinnamon,cloves, and cumin showed the strongest antimicrobial effectsagainst Staphylococcus aureus, Klebsiella pneumonia, Pseudomonasaeruginosa, Escherichia coli, Enterococcus faecalis, Mycobacteriumsmegmatis, Micrococcus luteus, and Candida albicans as test strains,with inhibition zones between 30 mm by the disc-diffu-sion method (Agaoglu, Dostbil, & Alemdar, 2007).

a-Pinene, cineole, limonene, linalool and geranyl acetate are vecommon antimicrobial compounds that have been effective againstsome food-borne pathogens and antibiotic-resistant Staphylococcusaureus, Bacillus cereus, Escherichia coliandCampylobacter jejuni (Chenet al., 2008; Sandasi et al., 2008). Spices such as allspice, bay leaf, car-away, coriander, cumin, cassiabarkand liquoricehavebeenreportedto have signicant bacteriostatic/inhibition properties for patho-

Table 1Spices, herbs and oils with antimicrobial activity and their avor components. Source:

Category Species Plant part

Herbs Basil, sweet (Ocimum basilicum) LeavesOregano (Origanum vulgare) Leaves/oweRosemary (Rosmarinus ofnicalis) LeavesSage (Salvia ofcinalis) LeavesThyme (Thymus vulgares) Leaves

Spices Allspice, pimento (Pimenta diocia) Berry/leavesCinnamon (Cinnamonum zeylanicum) BarkClove (Syzgium aromaticum) Flower budMustard (Brassica) SeedNutmeg (Myristica fragrans) SeedVanilla (Vanilla planifola, V. pompona, V.tahitensis)

Fruit/seedOils Olive oil FruitTea-tree oil (Melaleuca alternifolia) Leavesence in antimicrobial/antioxidant activity of the Tunisian Thymuscapitatus Hoff. et Link (Bounatirou et al., 2007). The antimicrobialactivity of the eugenol oil (Eugenia caryophylata) containing pheno-lic compounds is considerably lower compared to similar chemicalcompounds (Amiri, Dugas, Pichot, & Bompeix, 2008). Allyl isothio-cyanate is a non-phenolic volatile compound that showed similareffect at 9.4 ppm as mustard EOs in the culture medium with12.3 ppm of the puried component (Turgis, Han, Caillet, & Lacroix,2009). The presence of multiple phenolic phytochemicals from se-lected clonal herb species of the Lamiaceae family could preventStaphylococcus aureus from developing antimicrobial resistance(Kwon, Apostolidis, Labbe, & Shetty, 2007).

More than 400 spices have been used in theworld,mostly in hot-climate countries (Ceylan & Fung, 2004). There are a variety of effec-tive antimicrobial components in EOs derived from herbs such asoregano and thyme: carvacrol and p-cymene are two of them (Burtet al., 2007). Application of yarrow (Achillea. millefolium) as an an-cient spice showed antimicrobial effect at 30% concentration againstStaphylococcus aureus and Escherichia coli (Tajik& Jalali, 2009). Oreg-ano and thyme, oregano with marjoram, and thyme with sage hadthe most effective EOs against Bacillus cereus, Pseudomonas aerugin-osa, Escherichia coli O157:H7 and L. monocytogenes (Almajano et al.,2008; Graumann & Holley, 2008; Gutierrez et al., 2008a; Naidu,2000a; Tolonen et al., 2004). Phenolic compounds of spices, whichcontain a high percentage of eugenol, carvacrol and/or thymol, areprimarily responsible for bacteriocidal/bacteriostatic properties(Gutierrez, Rodriguez, Barry-Ryan, & Bourke, 2008b; Gutierrezet al., 2008a; Mandalari et al., 2007; Naidu, 2000b; Olonisakin, Ola-dimeji, & Lagide, 2007; Rodrguez et al., 2009).

Table 1 presents some antimicrobial activities and componentsof spices and herbs.

apted from Ceylan and Fung (2004), Holley et al. (2005), and Naidu (2000a).

Major avor component Bacterial inhibition (%)

Linalool/methyl chavicol

Con4.1. Mechanism of action

It has beendemonstrated that the antimicrobial effects of the EOsacts by causing structural and functional damages to the bacterialcellmembrane. It is also indicated that the optimumrange of hydro-phobicity is involved in the toxicity of the EOs (Goni et al., 2009).

Spices and herbs are mostly used in the range of 0.050.1%(5001000 ppm) in food systems. Some spices have stronger anti-microbial activity than others and can be effective at 1000 ppm.However, some spices require higher concentrations (Ceylan &Fung, 2004). Application of antimicrobials by different exposuremethods, such as vapor phase compared to direct contact method,of mustard and clove EOs showed noteworthy differences (Goniet al., 2009). The stereochemistry, lipophilicity and other factors af-fected the biological activity of these compounds which might bealtered positively or negatively by slight modications (Veluri,Weir, Bais, Stermitz, & Vivanco, 2004). It has been shown that plantsubstances affect microbial cells by various antimicrobial mecha-nisms, including attacking the phospholipid bilayer of the cellmembrane, disrupting enzyme systems, compromising the geneticmaterial of bacteria, and forming fatty acid hydroperoxidasecaused by oxygenation of unsaturated fatty acids (Arques et al.,2008; Burt et al., 2007; Lanciotti et al., 2004; Proestos et al.,2008; Silva et al., 2007; Skocibusic et al., 2006). Allyl isothiocya-nate derived from mustard seems to have multi-targeted mecha-nisms of action in metabolic pathways, membrane integrity,cellular structure and statistically signicant higher release of thecell compounds of Escherichia coli O157:H7 (Turgis et al., 2009).

Carvacrol increases the heat shock protein 60 HSP 60 (GroEL)protein and inhibited the synthesis of agellin highly signicantlyin E. coli O157:H7 (Burt et al., 2007). There are concerns regardingthe enhanced aroma and taste of oregano at the higher levels ofapplication in food items, especially at 1% (Chouliara, Karatapanis,Savvaidis, & Kontominas, 2007). The inuence of seasonal harvestof plants, geographical location and altitude, storage and extractionprocedures still has to be investigated in detail in order to be able todraw the utmost benet for nutritional and evenmore for industrialuse (Proestos et al., 2008; Silva et al., 2007). Seasonal variationsmight have some effects on EOs of the cerrado species (Silva et al.,2007); however, they did not have a signicant effect on the EOs de-rived from Myrcia myrtifolia (De Cerqueira et al., 2007). The crudeextract of Sorghum bicolorMoench has useful antimicrobial proper-ties and plant extract and fractions showed variable antimicrobialproperties (Kil et al., 2009). Table 2 lists some of these compounds,their reported plant origins and antimicrobial effects. Generally,higher concentrations of EOs are necessary in food, compared toin vitro trials: twofold differences in semi-skimmilk, 10-fold in porkliver sausage, 50-fold in soup and 25100-fold in soft cheese. How-ever, for Aeromonas hydrophila there was no difference betweenin vitro and in-food experiments on cooked pork and lettuce (Burt,2004; Naidu, 2000a). The apparent antimicrobial efcacy of plant-origin antimicrobials depends on factors such as the method ofextracting EOs from plantmaterial, the volume of inoculum, growthphase, culture medium used, and intrinsic or extrinsic properties ofthe food such as pH, fat, protein, water content, antioxidants, pre-servatives, incubation time/temperature, packaging procedure,and physical structure of food (Brandi et al., 2006; Burt, 2004;Lis-Balchin, Steyrl, & Krenn, 2003; Lopez-Malo vigil et al., 2005). An-other important parameter regarding effects of food preservatives isability to reduce the pH level inside the bacterial cell (pHin). It hasbeen shown that pHin of both E. coli and Salmonellahas been reducedby the effect of mustards EOs (Turgis et al., 2009).

Generally, Gram-negative bacteria are less sensitive to the anti-

M.M. Tajkarimi et al. / Foodmicrobials because of the lipopolysaccharide outer membrane ofthis group, which restricts diffusion of hydrophobic compounds.However, this does not mean that Gram-positive bacteria are al-ways more susceptible (Burt, 2004). Gram-negative bacteria areusually more resistant to the plant-origin antimicrobials and evenshow no effect, compared to Gram-positive bacteria (Rameshku-mar, George, & Shiburaj, 2007; Stefanello et al., 2008).

4.2. Synergistic and antagonistic effects of components

When the combined effect of substances is higher than the sumof the individual effects, this is synergy; antagonism happens whena combination shows less effect compared to the individual appli-cations (Burt, 2004). Synergistic effects of some compounds, inaddition to the major components in the EOs, have been shownin some studies (Abdalla, Darwish, Ayad, & El-Hamahmy, 2007;Becerril, Gomez-Lus, Goni, Lopez, & Nerin, 2007; Rota, Herrera,Martinez, Sotomayor, & Jordan, 2008). Application of a certaincombination of carvacrol-thymol can improve the efcacy of EOsagainst pathogenic micro-organisms (Lambert, Skandamis, Coote,& Nychas, 2001).

Synergismbetween carvacrol and p-cymene, a veryweak antimi-crobial, might facilitate carvacrols transportation into the cell bybetter swelling the B. cereus cell wall (Burt, 2004). Antimicrobialactivity of combination of cinnamon and clove EOs in vapor phaseshowedbetter antimicrobialwith less activeconcentration in theva-por phase compare to liquid phase (Goni et al., 2009). Thymol andcarvacrol showed synergistic and antagonistic effects, in differentcombinations of cilantro, coriander, dill and eucalyptus EOs (eachcontaining several components) and mixtures of cinnamaldehydeand eugenol, against Staphylococcus sp.,Micrococcus sp., Bacillus sp.and Enterobacter sp. (Burt, 2004). An antagonistic effect on Bacilluscereuswas seen in ricewhencarvacrol andp-cymenewereusedwithsalt; high-hydrostatic pressure showeda synergistic effect in combi-nation with thymol and carvacrol against L. monocytogenes (Burt,2004). Vacuum packing in combination with oregano EOs showeda synergistic effect against L. monocytogenes with 23 log10 reduc-tion. Similar results have been recorded when clove and corianderEOs have been used against Aeromonas hydrophila on vacuum-packed pork. Application of oregano EO has a synergistic effect inmodied-atmosphere packaging (MAP) including 40% CO2, 30% N2and 30% O2 (Burt, 2004). The available oxygen is another factorantagonistic on EO activities; by decreasing the oxygen level, thesensitivity of micro-organisms to the EOs has been increased (Burt,2004). Residual hydrosols after distillation of EOs fromplantmateri-als can be used as economical sources of antimicrobial components(Lis-Balchin et al., 2003). Table 3 summarizes the results of variousexperiments regarding application of plant-origin antimicrobialsin food. Table 4 demonstrates some aspects and studies in the areaof plant-derived antimicrobials; due to methodological differences,such as choice of plant extract(s), test micro-organism(s) and anti-microbial test method, these ndings are not directly comparable.

Application of nisin with carvacrol or thymol has been positivelyeffective against Bacillus cereus with temperatures increasing from8 C to 30 C (Burt, 2004). Application of nisinwith rosemary extractenhanced the bacteriostatic and bactericidal activity of the nisin(Thomas & Isak, 2006). Oregano EOs, in combination with modi-ed-atmosphere packaging, have effectively increased the shelf lifeof fresh chicken (Chouliara et al., 2007). Antimicrobial resistance didnot develop in Yersinia enterocolitica and Salmonella choleraesuisafter sub-inhibitory passes with cinnamon, by direct contact or va-por phase (Goni et al., 2009). Combination of linalool and 1, 8cine-ole (1:1) created more resistance in E. coli, compared to applicationof pure linalool. Either synergism or antagonism of 1, 8-cineoleand linaloolderived fromCinnamosma fragrans couldhappenagainstGram-negative bacteria and Fusarium oxysporu (Randrianarivelo

trol 21 (2010) 11991218 1203et al., 2009). The synergistic effect of different components could of-fer a way to prevent possible off avor caused by clove and tea treewhen used to protect against Escherichia coliO157:H7 andminimize

d Gmo

lostristeruri

s Baichialm

ConTable 2Some reported sources of natural antimicrobials in plant within the last 10 years.

Plant name Effective against

Coriander (Coriandum sativum), Oregano (Origanum vulgare),Rosemary (Rosmarinus ofcinalis), Parsley (Petroselinumcrispum)

Gram-positive anincluding Listeria

Allipse (Pimenta dioica), Basil (Ocimum basilicum), Blue mallee(Eucalyptus polybractea), Bay (Laurus nobilis), Carawayseed (Carum carvil), Lemongrass (Cymbopogon citratus),Lemon balm(Melissa ofcinalis), Marijoram (Origanummajorana), Rosemary(Rosmarinus ofcinalis), and Sage(Salvia ofcinalis)

Bacillus subtilis, CEscherichia coli, LSalmonella typhimaureus

Clove (Syzygium aromaticum) Sage (Salvia ofcinalis),Cinnamon (Cinnamomum zeylanicum) and Marijoram(Origanum majorana), Allipse (Pimenta dioica)

Pathogens such abotulinum, Eschermonocytogenes, S

1204 M.M. Tajkarimi et al. / Foodoff avor effects in meat products (Moriera et al., 2007). Combina-tions of EOs of oregano and thyme, oregano with marjoram andthymewith sage had themost effects against Bacillus cereus, Pseudo-monas aeruginosa, Escherichia coli O157:H7 and L. monocytogenes(Gutierrez et al., 2008a).

5. Review of some ndings of in vitro experiments

In vitro experiments on plant-origin antimicrobials are well de-scribed in the literature. However, the antimicrobial activity ofherbs and spices might vary based on the tested organism (Baga-mboula, Uyttendaele, & Debevere, 2003). Below are some examplesof reported ndings organized by the target microbial species.

5.1. A. hydrophila

This is the most sensitive to antimicrobials among Gram-nega-tive species (Burt, 2004). Linalool and methyl chavicol vanillin ex-

Staphylococcus aureu

Basil (Ocimum basilicum), Bay (Laurus nobilis), andLemongrass (Cymbopogon citratus)

Broad spectrum antibGram-positive and Gpathogenic micro-org

Blackberry (Rubus spp.), Bay (Laurus nobilis), Basil (Ociumbasilicum), Cilantro (immature leaves of Coriandrumsativum), Coriander (Coriandrum sativum seeds),Cinnamon (Cinnamomum zeylanicum), Coriander(Coriandum sativum), Marijoram (Origanum majorana) andThyme (Thymus vulgaris)

Staphylococcus spp.

Oregano (Origanum vulgare), Sage (Salvia ofcinalis), Thyme(Thymus vulgaris) and Satureja hortensis L.

Staphylococcus aureu

Marjoram (Origanum majorana) Alternative for synthroutinely used in the

Cumin (Cuminum cyminum) Bacillus cereus, Bacillubotulinum, Listena moPseudomonas uorescenteritidis, Staphyloco

Dill (Anethum graveolens) Clostridium botulinumaeruginosa, Staphylocenterocolitica

Fennel (Foeniculum vulgare) Bacillus cereus, ClostrSalmonella enteritidisYersinia enterocolitica

Garlic (Allium vineale) Broad spectrum antibGram-positive and Gpathogenic micro-org

Mint (Mentha piperita) Broad spectrum antibGram-positive and Gpathogenic micro-org

Onion (Allium cepa) Escherichia coli, SalmoShigella dysenteriae, SReference

ram-negative bacteria,nocytogenes

Angioni et al. (2004), Ceylan and Fung (2004),Daferera et al. (2000), El-Zemity, Radwan, El-Monam,and Sherby (2008), Gutierrez et al. (2008a, 2008b),Kim, Wei et al. (1995), Lopes-Lutz et al. (2008), andSantos and Rao (2001)

idium botulinum,ia monocytogenes,um and Staphylococcus

Angioni et al. (2004), Burt (2004), Ceylan and Fung(2004), Daferera et al. (2000), El-Zemity et al. (2008),Greule and Mosandl (2008), Gutierrez et al. (2008a),Gutierrez et al. (2008b), Kim , Wei et al. (1995),Lopes-Lutz et al. (2008), Lopez-Malo vigil et al.(2005), and Santos and Rao (2001)

cillus subtilis, Clostridiuma coli, Listeriaonella typhimurium,

Amiri et al. (2008), Burt (2004), Ceylan and Fung(2004), Greule and Mosandl (2008), Gutierrez et al.(2008a, 2008b), Ho, Wang, Wei, Lu, and Su (2008),

trol 21 (2010) 11991218tracted from sweet basil vanilla showed an inhibitory effect on A.hydrophila at 0.125% v/v methyl chavicol, 1% v/v linalool (Davidson& Naidu, 2000).

5.2. Bacillus sp.

Bacillus sp. were inhibited by: guarana extract (Majhenic,Skerget, & Knez, 2007), EOs of Syzygium gardneri leaves (Raj,George, Pradeep, & Sethuraman, 2008), supercritical uid extractof the shiitake mushroom Lentinula edodes (Kitzberger, Smania,Pedrosa, & Ferreira, 2007), hydro-distilled fresh leaves of Pittospo-rum neelgherrense Wight et Arn (John, George, Pradeep, & Sethur-aman, 2008), leaves, bark and fruits of Neolitsea scheri (Johnet al., 2008), EOs of the ower heads and leaves of Santolina ros-marinifolia L. (Compositae) (Ionnouy et al., 2007), different ex-tracts of thyme, hydro distillation of Syzygium gardneri leaves(Raj et al., 2008), aerial parts of fresh Plectranthus cylindraceusoil (Mohsenzadeh, 2007), EOs of Actinidia macrosperma (Lu, Zhao,

s Kim, Wei et al. (1995), and Lopez-Malo vigil et al.(2005)

acterial effect againstram-negativeanisms

Ceylan and Fung (2004) and Skocibusic et al. (2006)

Burt (2004), Greule and Mosandl (2008), Gutierrezet al. (2008a, 2008b), Lopez-Malo vigil et al. (2005),and Romeo et al. (2008)

s and Escherichia coli Bousmaha-Marroki et al. (2007), Burt (2004), andRazzaghi-Abyaneh et al. (2008)

etic preservativesfood industry

Mahmoud et al. (2007)

s subtilis, Clostridiumnocytogenes,ens, Salmonellaccus aureus

Ceylan and Fung (2004)

, Pseudomonasoccus aureus, Yersinia


idium botulinum,, Staphylococcus aureus,






nella typhimurium,taphylococcus aureus


Table 3Inhibitory activities of plant-origin antimicrobials against pathogenic bacteria, protein toxins and fungi, listed alphabetically representative studies conducted within the last10 years.

Organism Adverseeffects

Inhibitors References

Bacillus cereus Foodpoisoning;emesis

Tea, eugenol, leaf volatile oil, bark volatile oil; barkoleoresin, E-cinnamaldehyde, clove, mustard, cinnamon,Melianthaceae (Bersama engleriana), oil-maceratedgarlic, Petiveria alliacea L. root extract, Aristolochia indicaL., tannins, dried and commercial garlic products, garlicoil, marjoram and basil essential oils, citral, linalool andbergamot vapor, methanol and acetone extracts of 14plants belonging to different families

Arques et al. (2008), Fisher and Philips (2008),Friedman, Henika, Levin, Mandrell (2006), Friedman,Henika, Levin, Mandrell, and Kozukue (2006),Gutierrez et al. (2008a), 2008b), Kim et al. (2006),Kuete et al. (2008), Lopez et al. (2007), Majhenic et al.(2007), Singh, Maurya, De Lampasona, and Catalan(2007), Vagahasiya and Chanda (2007), Winwardet al. (2008), Yoshida et al. (1999), and Yilmaz (2006)

Bacillus subtilis Foodpoisoning

Teas, leaf volatile oil, leaf oleoresin, eugenol, barkvolatile oil; bark oleoresin, E-cinnamaldehyde, oil-macerated garlic extract, tannins, polymers of avanols,cassia bark-derived substances, crude extracts of bulbs(Lycoris chinensis), stems and leaves of (Nandinadomestica), (Mahonia fortunei), (Mahonia bealei), stems ofBerberis thunbergii and stems, leaves and fruits ofCamptotheca acuminata, methanol and acetone extractsof 14 plants belonging to different families

Kong, Wang, and Xiong (2007), Li, Zhu et al. (2008),Singh et al. (2007), Vagahasiya and Chanda (2007),Yoshida et al. (1999), and Yilmaz (2006)

Campylobacter jejuni Foodpoisoning;diarrhea

Black and green tea, cinnamaldehyde and carvacrol Friedman (2007), Arques et al. (2008), andRavishankar, Zhu, Law, Joens, and Friedman (2008)

Escherichia coli Foodpoisoning;diarrhea

Cinnamon, oregano oil (Oreganum vulgare), pureessential oils, leaf volatile oil, eugenol, bark volatile oil,bark oleoresin, E-cinnamaldehyde, carvacrol, oreganooil, citra, lemongrass oil, cinnamaldehyde, cinnamon oil,[Oregano in whey protein isolate (WPI) lms containing,at 2% level, garlic essential oil at 3&4%], lemongrass,thyme, carvacrol, cinnamaldehyde, citral, and thymol,clove (Eugenia caryophyllata), glucosinolates naturallypresent in mustard powder, mustard, Bersamaengleriana (Melianthaceae), chrysanthemum extracts,cabbage juice, Petiveria alliacea L. roots, Aristolochiaindica L., catechin, chlorogenic acid and phloridzin,ground yellow mustard, Brassica oleracea juice, driedgarlic powder, commercial garlic products, and garlic oil,onion, marjoram and basil essential oils, Scutellaria,Forsythia suspensa (Thunb), and rosemary and clove oilwith 75% ethanol, cassia bark-derived substances, thyme(Thymus vulgaris), bay (Pimenta racemosa), ion extracts,lemongrass, crude extracts of Lycoris chinensis (bulbs),Nandina domestica/Mahoniafortunei/Mahonia bealei(stems and leaves), Berberis thunbergii (stems) andCamptotheca acuminata (stems, leaves and fruits),methanol and acetone extracts of 14 plants belonging todifferent families, caffeine, 1,3,7-trimethylxanthine.

Arques et al. (2008), Becerril et al. (2007), Ben Sassi,Harzallah-Skhiri, Bourgougnon, and Aouni (2008),Davidson and Naidu (2000), Falcone et al. (2005),Ghosh, Kaur, and Ganguli (2007), Graumann andHolley (2008), Gutierrez et al. (2008a, 2008b),Hammer et al. (1999), Ibrahim, Salameh,Phetsomphou, Yang, and Seo (2006), Ibrahim, Yang,and Seo (2008), Kim, Wei et al. (1995), Kim et al.(2008), Knight and McKellar (2007), Kong et al.(2007), Kuete et al. (2008), Kyung and Lee (2001), Li,Zhu et al. (2008), Majhenic et al. (2007), Rojas-Grauet al. (2007), Singh et al. (2007), Seydim and Sarikus(2006), Sivakami and Rupasinghe (2007), Tolonenet al. (2004), Vagahasiya and Chanda (2007), andWinward et al. (2008)

Listeria monocytogenes Foodpoisoning;listeriosis

Tea, pure essential oils, [Oregano in whey protein isolate(WPI) lms containing at 2% level, garlic essential oil at3&4%], cabbage juice, cinnamon bark, cinnamon leaf, andclove, Brassica oleracea juice, lemon balm and sageessential oils, cassia bark-derived substances, citral,linalool and bergamot vapor

Brandi et al. (2006), Cava et al. (2004), Fisher andPhillips (2008), Friedman (2007), Gutierrez et al.(2008a, 2008b), Kong et al. (2007), Lopez et al. (2007),Seydim and Sarikus (2006), and Tolonen et al. (2004)

Mycobacterium tuberculosis Tuberculosis Catechins, Bersama engleriana (Melianthaceae) Friedman (2007), Kuete et al. (2008)

Pseudomonas aeruginosa Food spoilage Tea extract, [Milk protein-based edible lms containingoregano, 1.0% (w/v), pimento, or 1.0% oregano pimento(1:1)], tannins, polymers of avanols, lemongrass,oregano and bay, crude extracts of Lycoris chinensis(bulbs), Nandina domestica/Mahoniafortunei/Mahoniabealei (stems and leaves), Berberis thunbergii (stems)and Camptotheca acuminata (stems, leaves and fruits),certain combinations of carvacrol-thymol, oreganoessential oil; methanol and acetone extracts of 14 plantsbelonging to different families

Friedman (2007), Hammer et al. (1999), Lambert et al.(2001), Li et al. (2008), Oussalah et al. (2004), andYilmaz (2006)

Pseudomonas uorescens Food spoilage Teas, [Milk protein-based edible lms containingoregano, 1.0% (w/v) pimento, or 1.0% oreganopimento(1:1)], tannins, polymers of avanols

Friedman (2007), Oussalah et al. (2004), and Yilmaz(2008)

Shigella spp. Tea Diarrhea Tea, Bersam engleriana(Melianthaceae), tannins,polymers of avanols, crude extracts of Lycoris chinensis(bulbs), Nandina domestica/Mahonia fortunei/Mahoniabealei (stems and leaves), Berberis thunbergii (stems)and Camptotheca acuminata (stems, leaves and fruits)

Arques et al. (2008), Friedman (2007), Kuete et al.(2008), Li, Zhu et al. (2008), and Yilmaz (2006)

(continued on next page)

M.M. Tajkarimi et al. / Food Control 21 (2010) 11991218 1205

oleo, E-cPI)3&4innas vd th(Co), Ared g

ConTable 3 (continued)

Organism Adverseeffects

Inhibitors

Salmonella spp. Foodpoisoning;Salmonellosis

Teas, leaf volatile oil; leafvolatile oil; bark oleoresinin whey protein isolate (Wlevel, garlic essential oil atvulgare), and cinnamon (Clemongrass, thyme (Thymucinnamaldehyde, citral, anof Aspilia mussambicensisengleriana (MelianthaceaeBrassica oleracea juice, dri

1206 M.M. Tajkarimi et al. / FoodWang, Chen, & Fu, 2007), specic derivative from the fruits ofEucalyptus globulus (Tan et al., 2008), EOs from thymol and carva-crol at1:2000 dilutions and cinnamic aldehyde and eugenol ex-tracted from cinnamon and clove at 0.11.0% w/v, 0.06% v/vconcentration(Davidson & Naidu, 2000), aerial parts of Ammoidesatlantica (Coss. et Dur.) Wolf. (Apiaceae) (Laouer et al., 2008),leaves, bark and fruits of Neolitsea scheri (John et al., 2008), hy-dro-distilled dried and oil samples of Thymus caramanicus (NejadEbrahimi et al., 2008), and EOs from Anzer teas and wild-grownleaves of Acorus calamus (Radusiene, Judzentiene, Peciulyte, &Janulis, 2007; Sekeroglu, Deveci, Buruk, Gurbuz, & Ipek, 2007).Extracts of different spices, evaluated by disc diffusion assay,had the following relative inhibitory effects on Bacillus cereus:clove > mustard > cinnamon > garlic > ginger > mint (Soa et al.,2007).

garlic products, and garlic oil,essential oils, cassia bark-derivlemongrass, bay, methanol andplants belonging to different fa

Spore forming bacteria Foodpoisoning

Catechins

Staphylococcus aureus Foodpoisoning;infection

Theasinensin, tea, cinnamon, ovulgare), pure essential oils, leaeugenol, bark volatile oil, barkcinnamaldehyde, [oregano in wlms containing at 2% level, gar4%], dried garlic powder, commclove, mustard, rosemary (Rosmbalm (Melissa ofcinalis), sage (Smint (Mentha piperata), and oreBersama engleriana (Melianthaextracts, oil-macerated garlic eroot extract, Aristolochia indicaavanols, lemongrass and bay;carvacrol- thymol, citral, linalooacetone extracts of 14 plants befamilies

V. cholerae Cholera Tea extract

V. parahaemolyticus Mild gastro-enteritis

Basil, clove, garlic, horseradishrosemary, thyme, cassia bark-d

Yersinia enterocolitica Diarrhea Teas, pure essential oils

ToxinsBotulinum Neurotoxin

botulismBlack tea

Cholera Cholera Catechins, theaavins

MoldsAspergillus avus Myco-

toxicosisPure essential oils, leaf oleoreseugenol, bark volatile oil, barkcinnamaldehyde, cassia bark-d

Aspergillus niger Ochratoxins Methanol extract of Aspilia mu(Compositae)

Aspergillus parasiticus Myco-toxicosis

ThymolReferences

resin; eugenol; barkinnamaldehyde, [oreganolms containing at 2%%], oregano (Origanummomum zeylanicum),ulgaris), carvacrol,ymol), methanol extractmpositae), Bersamaistolochia indica L.,arlic powder, commercial

Davidson and Naidu (2000), Friedman (2007),Gutierrez et al. (2008a), 2008b), Hammer et al.(1999), Kong et al. (2007), Kuete et al. (2008), Singhet al. (2007), Seydim and Sarikus (2006), Vagahasiyaand Chanda (2007), and Yoshida et al. (1999)

trol 21 (2010) 119912185.3. C. jejuni

It has been shown that Campylobacter jejuni is more sensitiveto natural antimicrobials compared to other pathogenic micro-organisms (Sudjana et al., 2009). Linalool vapor of bergamotand linalool oils (Fisher & Phillips, 2008), cinnamic aldehydeand eugenol extracted from cinnamon and clove at 0.05% con-centration, linalool and methyl chavicol vanillin extracted fromsweet basil vanilla at 0.25% concentration (Davidson & Naidu,2000). EO of Origanum minutiorum with a capacity as a foodpreservative showed a variety of antimicrobial effects againstCampylobacter jejuni (Aslim & Yucel, 2007). The ciprooxacinresistance of Campylobacter strains has been shown to bestrongly diminished by application of EO of Origanum minutio-rum (Aslim & Yucel, 2007).

marjoram and basiled substances,acetone extracts of 14milies, thymol

Friedman (2007)

regano (Origanumfvolatile oil, leaf oleoresin,oleoresin, E-hey protein isolate (WPI)lic essential oil at 3% andercial garlic products,arinus ofcinalis), lemonalvia ofcinalis), chocolategano (Origanum vulgare),ceae), chrysanthemumxtract, Petiveria alliacea L.L., tannins, polymers ofcertain combinations ofl andvapor,methanolandlonging to different

Arques et al. (2008), Ben Sassi et al. (2008), Fisher andPhillips (2006), Friedman (2007), Gutierrez et al.(2008a), Gutierrez et al. (2008b), Hammer et al.(1999), Kuete et al. (2008), Kwon et al. (2007),Lambert et al. (2001), Lopez et al. (2007), Musyimiet al. (2008), Singh et al. (2007), Seydim and Sarikus(2006), Vagahasiya and Chanda (2007), Winwardet al. (2006), Yilmaz (2006), and Yoshida et al. (1999)

Arques et al. (2008)

, marjoram, oregano,erived substances

Kong et al. (2007) and Yano et al. (2006)

Friedman (2007), Lopez et al. (2007)

Friedman (2007)

Friedman (2007)

in, leaf volatile oil,oleoresin, E-erived substances

Kong et al. (2007) and Lopez et al. (2007)

ssambicensis Musyimi et al. (2008)

Davidson and Naidu (2000)

Table 4Some studies regarding application of EOs or their components in-food studies conducted in the past 10 years.

Food group EO or component Bacterial species Inhibitory effect Reference

Meat and poultryMeat Clove oil , eugenol and coriander, oregano,

thyme oils, encapsulated rosemary EO,clove and tea tree

Listeria monocytogenes,Aeromonas hydrophila,Escherichia coli O157:H7

Yes (+++) Burt (2004) and Moriera et al.(2007)

Fried meat Oregano and thyme, oregano withmarjoram and thyme with sage

B. cereus and P. aeruginosa,Escherichia coli O157:H7 andListeria monocytogenes

Yes (+) Du and Li (2008)

Ground beef Chinese cinnamon and winter savory EOs Pathogenic micro-organisms Yes (increased radio-sensitivity)

Turgis et al. (2008)

Meat EOs and nisin Listeria monocytogenes Yes Solomakos et al. (2008)

Meat surfaces Oregano, pimento, or oregano:pimento Escherichia coli O157:H7 orPseudomonas spp.

Yes Mosqueda-Melgar et al. (2008a,2008b), and Oussalah et al. (2004)

Fresh sausage Marjoram (Origanum majorana L.) EO Several species of bacteria Yes Burt (2004)

Chicken Eugenol Listeria monocytogenes,Aeromonas hydrophila,

Yes (+++++) Burt (2004)

Chicken Sage oil Bacillus cereus, Staphylococcusaureus, Salmonella typhimurium

No Burt (2004)

Chicken Oregano Increase shelf life Yes (with modied-atmospherepackaging)

Chouliara et al. (2007)

Pate Mint oil Listeria monocytogenes,Salmonella enteritidis

No Burt (2004)

Minced pork Thyme oil Listeria monocytogenes No Burt (2004)

Vacuum-packed ham Cilantro oil Listeria monocytogenes No Burt (2004)

Vacuum-packedminced pork

Oregano oil Clostridium botulinum spores No Burt (2004)

Liver pork sausage Rosemary Listeria monocytogenes Yes (encapsulatedhas more effect thanstandard)

Hayouni, Chraief et al. (2008)

Minced pork Winter savory (Satureja montana) EO Food-borne bacteria andimprove quality

Yes (in combinationwith othertechniques)

Carraminana et al. (2008)

FishCooked shrimp Thyme oil, cinnamaldehyde Pseudomonas putida Very slight Burt (2004)

Red grouper llet,cubed

Carvacrol, citral, geraniol Salmonella typhimurium Yes (+++) Burt (2004)

Cod llets Oregano oil Photobacterium phosphoreum Yes (+) Burt (2004)

Salmon llets Oregano oil Photobacterium phosphoreum No Burt (2004)Cods roe salad Mint oil Salmonella enteritidis Yes (+++) Burt (2004)

Coated semi-friedtuna slices

Eugenol and linalool Increased shelf life Yes Naidu (2000a)

Fresh-water sh Wild-thyme hydrosol Increased shelf life, preservativeeffect

Yes Oral et al. (2008)

Lightly saltedcultured seabream (Sparusaurata) llets

Oregano Increased shelf life, antioxidantactivity

Yes Goulas and Kontominas (2007)

Carp llets Carvacrol + Thymol Four times increased shelf life Yes Mahmoud, Kawai, Yamazaki,Miyashita, and Suzuki (2006)

Carp Thymol, carvcarol and cinnamaldehyde Increased shelf life Yes (+++) Mahmoud et al. (2004)

Carp Allyl isothiocyanate, carvacrol,cinnamaldehyde, citral, cuminnaldehyde,eugenol, isoeugenol, linalool and thymol

Increased shelf life Yes (+) Mahmoud et al. (2004)

DairyMozzarella cheese Clove oil Listeria monocytogenes Yes (+) Burt (2004)

Semi-skimmed milk Carvacrol Listeria monocytogenes Yes (+) Burt (2004)

Soft cheese DMC Base Natural preservativecomprising 50% EOs of rosemary, sage andcitrus

Listeria monocytogenes From 1.0 ll g1(+) Burt (2004)

(continued on next page)

M.M. Tajkarimi et al. / Food Control 21 (2010) 11991218 1207

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7:H

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ConTable 4 (continued)

Food group EO or component Bacterial s

Yoghurt Clove, cinnamon, cardamom, peppermintoil

Streptococc

Tzatziki (yogurt andcucumber salad)

Mint oil Salmonella

Butter Satureja cilicica essential oil Antioxidan

Dairy industries Oregano, thyme, rosemary, sage, cuminand clove

Starter culspoilage

VegetablesLettuce, romaine Thyme oil E. coli O15

Carrots Thyme oil E. coli O15

Lettuce, iceberggreen

Basil methyl chaviol (BMC) Natural o

Eggplant salad Oregano oil E. coli O15

Alfalfa seeds Cinnamaldehyde, thymol Salmonella

RiceBoiled rice Carvacrol Natural o

Boiled rice Sage oil Bacillus ceraureus, Sal

Rice Ocimum basilicum Three stor(Sitophilusdominica apusillus)

FruitKiwifruit Carvacrol, cinnamic acid Natural o

Honeydew melon Carvacrol, cinnamic acid Natural o

1208 M.M. Tajkarimi et al. / Food5.4. Clostridium perfringens

Clove EOs have an inhibitory effect against Clostridium perfrin-gens at 0.4% (v/w) concentration (Davidson & Naidu, 2000).

5.5. Escherichia coli

A variety of antimicrobial effects on Escherichia coli has beenshown by: guarana extract (Majhenic et al., 2007), chloroform ex-tract of the plant of Abrus precatorious L. roots at 84% concentration(Zore et al., 2007), EOs from leaves, stems and owers of Salviareuterana (Lamiaceae) (Esmaeili et al., 2008), linalool vapor of ber-gamot and linalool oils (Fisher & Phillips, 2008),water-distilled EOfrom leaves and owers of Micromeria nubigena H.B.K. (Lamiaceae)(El-Seedi et al., 2008), hydro distillation leaf oil of Cinnamomumchemungianum (Raj et al., 2008), Rosmarinus ofcinalis oil (Gachkaret al., 2007), anzer tea EOs (Sekeroglu et al., 2007), EOs of Actinidiamacrosperma (Lu et al., 2007), oleuropein extracted from olive oil at0.4 mg/ml concentration; clove EOs at 0.4% (v/w) concentration;thymol and carvacrol EOs at 5%, 10%, 15%, 20% concentration, andcinnamic aldehyde and eugenol extracted from cinnamon andclove at 0.05% and 0.04% concentrations (Davidson & Naidu,2000), linalool and methyl chavicol vanillin extracted from sweetbasil vanilla at 0.25% concentration; terpenes extracted from tea-tree oil at 0.120.25% v/v concentration (Davidson & Naidu,2000), aerial parts of Ammoides atlantica (Coss. et Dur.) Wolf. (Api-aceae) (Laouer et al., 2008), mango seed kernel (Abdalla et al.,2007), EOs of the ower heads and leaves of Santolina rosmarinifoliaL. (Compositae) (Ionnouy et al., 2007), sorghum extracts and frac-tions (Kil et al., 2009), and hydro-distilled fresh leaves of Pittospo-rum neelgherrense Wight et Arn (John et al., 2008). Extracts and oilextracts of various spices had relative inhibitory effects on Esche-richia coli as follows: mustard > clove > cinnamon > garlic >ginger > mint (Soa et al., 2007).es Inhibitory effect Reference

hermophilus Yes (Mint oil +,Cardamom, clove:++, Cinamon:+++)

Burt (2004)

eritidis From 1.5%v/w ++ Burt (2004)

Yes Ozkan et al. (2007)

s and related food Yes Viuda-Martos et al. (2008)

7 Yes (+) Burt (2004)

7 Yes (+++) Burt (2004)Yes (++) Burt (2004)

7 Yes (++) Burt (2004)

., six serotypes Yes (50 C: +, 70 C:0)

Burt (2004)

Yes (+++) Burt (2004)

Staphylococcusella typhimurium

No Burt (2004)

ice pestsae, Rhyzopertharyptolestes

Yes Lopez et al. (2008)

Yes (+++) Burt (2004)

Yes (0+) Burt (2004)

trol 21 (2010) 119912185.6. L. monocytogenes

Rosmarinus ofcinalis oil showed a strong antimicrobial effectagainst L. monocytogenes (Gachkar et al., 2007). Thymol and carva-crol EOs showed inhibitory effects against L. monocytogenes at24 C in a microbiological medium at 0.50.7 w/v and were bacte-riostatic at 0.51.0% concentration; and borneol extracted fromsage and rosemary had inhibitory effect against L. monocytogenesat 0.020.05% concentration (Davidson & Naidu, 2000).

5.7. Molds and yeasts

Some EOs demonstrate a broad range of natural fungicidal ef-fects against post-harvest pathogens, especially because of theirbioactivity in the vapor phase for storage applications (Tripathi,Dubey, & Shukla, 2008). However, more time is needed for va-por-phase bioactivity effect, possible absorption into the foodmaterial needed to be considered (Fisher & Phillips, 2008). Anti-fungal activity might be affected by the targeted fungal physiolog-ical activity (Daferera et al., 2000).

The reported effective compounds against food-borne fungi,including Aspergillus niger; A. avus; and A. parasiticus are: guaranaextract (Majhenic et al., 2007), EO and methanol extract of Saturejahortensis (Dikbas, Kotan, Dadasoglu, & Sahin, 2008), Satureja hort-ensis L. containing carvacrol and thymol (Razzaghi-Abyanehet al., 2008), water-distilled EO from leaves and owers ofMicrom-eria nubigena H.B.K. (Lamiaceae) (El-Seedi et al., 2008), oleuropeinextracted from olive oil at 0.2 mg/ml concentration, EOs from thy-mol at 500 lg/ml concentration and at 1.0% and 100 lg/ml concen-trations; cinnamic aldehyde and eugenol extracted from cinnamonand clove at 1.0% and 100 lg/ml concentrations (Davidson & Nai-du, 2000), Aspergillus parasiticus growth and Aatoxins productionhas been inhibited by Thymus vulgari and Citrus aurantifolia,whereas Mentha spicata L., Foeniculum miller, Azadirachta indica A.

grass, have been more effective as volatiles (Suhr & Nielsen,

terial species such as Pseudomonas uorescens (Raj et al., 2008).

ConGuarana extract (Majhenic et al., 2007) and leaves, bark and fruitsof Neolitsea scheri (John et al., 2008) were active against Pseudo-monas uorescens.

5.9. Salmonella sp. and Shigella sp.

The below components has been reported as effective com-pounds against Salmonella sp. or Shigella sp: the oil isolated by hy-dro distillation of Syzygium gardneri leaves and leaf oil ofCinnamomum chemungianum (Raj et al., 2008), hydro-distilledEOs of fresh leaves and mature fruits of Pittosporum viridulum(John, Karunakaran, George, Pradeep, & Sethuraman, 2007), EOsof Iranian avoring, Zataria multiora Boiss(Akhondzadeh Basti,Misaghi, & Khaschabi, 2007), syringic acid, isorhamnetin and quer-cetin, three compounds extracted from dried fruit of Ardisia ellipti-ca Thunb (Phadungkit & Luanratana, 2006), oleuropein extract,cinnamic aldehyde and eugenol extracted from cinnamon andclove at 0.05% and 0.04% concentration, linalool and methyl chav-icol vanillin extracted from sweet basil vanilla at 0.1% concentra-tion , Terpenes extracted from tea-tree oil at 0.120.25% v/vconcentration (Davidson & Naidu, 2000), leaves bark and fruits of2003); however, in EOs such as marjoram oil, they have been effec-tively antifungal in a matrix with mainly hydrocarbons (Dafereraet al., 2000).

5.8. Pseudomonas sp.

Pseudomonas, specically Pseodumonas aeruginosa are the leastsensitive group of bacteria to the action of EOs and bioactive com-ponents of plant-origin (Burt, 2004; Ceylan & Fung, 2004). Bioac-tive components of plant-origin antimicrobials are relativelyweak against Pseudomonas spp. (Ceylan & Fung, 2004). However,susceptibility of all except Pseudomonas aeruginosa to the Origanumgenus has been shown (Bendahou et al., 2008).

Hydro-distilled EOs from leaves, stems and owers of Salviareuterana (Lamiaceae) (Esmaeili et al., 2008); clove EOs at 0.4%(v/w) concentration as well as EOs from thymol and carvacrol(Davidson & Naidu, 2000), leaves, bark and fruits of Neolitsea sc-heri (John et al., 2008), oils of air-dried samples obtained by hydrodistillation of Thymus caramanicus (Nejad Ebrahimi et al., 2008)were active against Pseudomonas spp.

Antibacterial activity of the oil isolated by hydro distillation ofSyzygium gardneri leaves was effective against Gram-negative bac-Juss, Conium maculatum and Artemisia dracunculus has only inhib-ited the fungal growth, while Carum carvi L. has controlled aa-toxin production without effect on the fungal growth (Razzaghi-Abyaneh et al., 2009), linalool and methyl chavicol vanillinextracted from sweet basil vanilla at 2000 lg/ml concentration(Davidson & Naidu, 2000) .

Hydro-distilled EOs of stems, leaves (at vegetative and ower-ing stages) and owers of Eugenia chlorophylla O. Berg. (Myrtaceae)(Stefanello et al., 2008), various extracts of thyme (Davidson & Nai-du, 2000; Nejad Ebrahimi et al., 2008), were active against moldsand yeasts. Oleoresin extracted from cinnamon and cinnamic alde-hyde and eugenol extracted from cinnamon and clove inhibitedmycotoxin-producing Aspergillus and Penicillium species at 2.0%w/v, 300 lg/ml concentrations (Davidson & Naidu, 2000).

Higher levels of phenolic compounds in thyme, cinnamon andclove showed antifungal effects. Smaller phenolic compounds,such as allyl isothiocyanate and citralon in mustard and lemon-

M.M. Tajkarimi et al. / FoodNeolitsea scheri (John et al., 2008, hydro-distilled EOs of freshleaves and mature fruits of Pittosporum viridulum (John et al.,2007).According to a study on MuellerHinton (MH) Agar and MHbroth, cloves showed antimicrobial effect against Shigella sonnei,Shigella exneri and E. coli at 1% weight/volume concentration (Bag-amboula et al., 2003).

5.10. Staphylococcus aureus

A variety of antimicrobial activities against Staphylococcusaureus:

Chloroform and ethanol fractions of Abrus precatorious L. rootswas 93% (percentage of inhibition) effective (Zore et al., 2007), hy-dro-distilled EOs from leaves, stems and owers of Salvia reuterana(Lamiaceae) (Esmaeili et al., 2008), EOs from an alpine needle leafof Abies koreana (Jeong, Lim, & Jeon, 2007), hydro-distilled extractof Syzygium gardneri leaves (Raj et al., 2008), hydro-distilled EOsof fresh leaves and mature fruits of Pittosporum viridulum (Johnet al., 2007), EOs from an alpine needle leaf of Abies koreana (Jeonget al., 2007), Rosmarinus ofcinalis oil (Gachkar et al., 2007); EOs ofZataria multiora Boiss (Akhondzadeh Basti et al., 2007), EOs ofActinidia macrosperma (Lu et al., 2007), oleuropein extracted fromolive at 0.1% w/v concentration of the extract delayed growth ofthe bacteria at 0.40.6% w/v concentration; clove EOs at 0.4% (v/w) concentration; EOs from thymol and carvacrol 5%, 10%, 15%,and 20% concentration, EOs from thymol and carvacrol at 175225 lg/ml concentration; cinnamic aldehyde and eugenol ex-tracted from cinnamon and clove at 0.03% and 0.04% concentra-tions, linalool and methyl chavicol vanillin extracted from sweetbasil vanilla at 0.1% concentration, terpenes extracted from tea-tree oil at 0.120.25% v/v concentration (Davidson & Naidu,2000), aerial parts of Ammoides atlantica (Coss. et Dur.) Wolf. (Api-aceae) (Laouer et al., 2008), leaves, bark and fruits of Neolitsea sc-heri (John et al., 2008), water-distilled EOs from leaves and owersof Micromeria nubigena H.B.K. (Lamiaceae) (El-Seedi et al., 2008),Curcuma domestica and Curcuma viridiora at ratios of 20/15 (Chenet al., 2008), anzer teas EOs (Sekeroglu et al., 2007), EOs of theower heads and leaves of Santolina rosmarinifolia L. (Compositae)(Ionnouy et al., 2007), and hydro-distilled EOs of fresh leaves andmature fruits of Pittosporum viridulum (John et al., 2007).

5.11. Vibrio parahaemolyticus

EOs from thymol and carvacrol at 0.5% concentration as wholespices and 100 lg/ml as essential oil (Davidson & Naidu, 2000),tannins and polymers of avanols (Yilmaz, 2006), and Curcumadomestica and Curcuma viridiora at ratios of 18/15 (Chen et al.,2008) showed antimicrobial activity against Vibrioparahaemolyticus.

5.12. General Gram-positive and Gram-negative bacteria

Mint (Mentha piperita) EO was more effective against S. enteriti-dis compared to L. monocytogenes when in Greek appetizers tara-mosalata and tzatziki. In another study, using freshly distilledEOs showed more susceptibility to Gram-positive bacteria com-pared to Gram-negative (Burt, 2004). Lemon, orange and bergamotEOs and their components (Fisher & Phillips, 2006), Hydro-distilledEOs of stems, leaves (at vegetative and owering stages) and ow-ers of Eugenia chlorophylla O. Berg. (Myrtaceae) are effectiveagainst Gram-positive bacteria (Stefanello et al., 2008).

Phlomis species from the Lamiaceae family, borneol extractedfrom sage and rosemary had an inhibitory effect against Gram-po-sitive and Gram-negative bacteria at 2% concentration for twogroups, 0.3% bacteriostatic and 0.5% bactericidal for Gram-positive

trol 21 (2010) 11991218 1209bacteria (Bajpai et al., 2008). Linalool and methyl chavicol vanillinextracted from sweet basil vanilla showed inhibitory effect against3335 bacteria, yeasts and molds (Davidson & Naidu, 2000).

Thymus zygis subsp. gracilis (thymol and two linalool chemotypes)

Finding the most inhibitory spices and herbs depends on a number

Conof factors such as type, effects on organoleptic properties, compo-sition and concentration and biological properties of the antimicro-bial and the target micro-organism and processing and storageconditions of the targeted food product (Gutierrez et al., 2008a;Naidu, 2000a; Romeo, De Luca, Piscopo, & Poiana, 2008). In a studyon blanched spinach and minced cooked beef, using clove and tea-tree EOs, three and four times the MIC in in vitro studies wereneeded to restrict E. coli O157:H7 populations in the food materials(Moriera et al., 2007). Despite some positive reports in regard toapplication of plant-origin natural antimicrobials, two major issuesare faced regarding application of plant-origin antimicrobials infood: odors created mostly by the high concentrations, and thecosts of these materials (Proestos et al., 2008; Silva et al., 2007).

6.1. Meat and poultry products

It has been shown that plant extracts are useful for reduction ofpathogens associated with meat products. However, some authorshave recorded low antimicrobial effects against pathogens in con-taminated meat products (Grosso et al., 2008). High-fat-content ofthe food materials has effects on the application of EOs (Burt,2004; Lis-Balchin et al., 2003). It may be because of the lipid solubil-and Thymus hyemalis L. (thymol, thymol/linalool and carvacrolchemotypes) was active against 10 pathogenic micro-organisms(Sabulal, George, Pradeep, & Dan, 2008). Generally, Gram-positivebacteria are more sensitive to saponin, with MIC (minimum inhibi-tory concentration) between 0.3 and 1.25 mg/ml, compared to1.255 mg/ml for Gram-negatives (Oleszek, 2000). MIC of oreganoEOswere lower than thyme and cinnamon EOs, against Gram-nega-tivepathogenicmicro-organisms (Escherichia coli, Yersinia enterocol-itica, Pseudomonas aeruginosa, and Salmonella choleraesuis)compared to Gram-positive ones (Listeria monocytogenes, Staphylo-coccus aureus, Bacillus cereus, and Enterococcus faecalis) as well asmolds (Penicillium islandicum and Aspergillus avus) (Lopes-Lutzet al., 2008; Lopez, Sanchez, Battle, & Nerian, 2007).

6. Some in-food experiments with plant-origin antimicrobials

In-food studies depend on several additional factors, whichhave not been tested in similar in vitro studies (Stoicov, Saffari, &Houghton, 2009). Spices and herbs can be used as an alternativepreservative and pathogen-control method in food materials.Application of both extracts and EOs of plant-origin antimicrobialssuch as oral parts of Nandina domestica Thunb could be a potentialalternative to synthetic preservatives (Bajpai et al., 2008).Generally, effective EOs in decreasing order of antimicrobial activ-ities are: oregano > clove > coriander > cinnamon > thyme > mint >rosemary > mustard > cilantro/sage (Burt, 2004). However, in an-other study, mint showed less antimicrobial effect compared tomustard (Soa et al., 2007). There are differences betweenin vitro and in-food trials of plant-origin antimicrobials, mainly be-cause only small percentages of EOs are tolerable in food materials.Bergamot peel (Mandalari et al., 2007) is effective against gram-negative bacteria. Origanumoil, extractedby steamdistillation fromThymus capitatus L. (Labiatae) by Hoffmanns and Link (commonname: Spanish oregano; synonyms: Coridothymus capitatus or Thy-mus capitatis), at 486 mg/L concentration in treated-grey-waterreed-bed efuent, can prevent coliform re-growth for up to 14 days(Winward, Avery, Stephenson, & Jefferson, 2008). Antimicrobialactivity of EOs extracted from Thymus vulgaris (thymol chemotype),

1210 M.M. Tajkarimi et al. / Foodity of EOs compared to aqueous parts of food (Lis-Balchin et al.,2003). Combination of 1% cloves and oregano in broth cultureshowed inhibitory effect against L. monocytogenes, however, thesame concentration was not effective in meat slurry (Lis-Balchinet al., 2003). According to Table 4, recent studies regarding certainoils such as eugenol and coriander, clove, oregano and thyme oilsshowed high effect against L. monocytogenes, Aeromonas hydrophilaand autochthonous spoilage ora in meat products. However, mus-tard, cilantro, mint and sage oils were less effective or ineffective(Burt, 2004). A 520 ll g1 level of eugenol and coriander, clove,oregano and thyme oil inhibits growth of L. monocytogenes, Aeromo-nas hydrophila and autochthonous spoilage ora in meat products(Burt, 2004).

Survival and growth of both susceptible and antibiotic-resistantCampylobacter strains have been inhibited effectively on agarplates and in contaminated ground beef by application of roselle(Hibiscus sabdariffa L.) (Yano, Satomi, & Oikawa, 2006; Yin & Chao,2008).

EOs activity inmeat products canbe reducedbyhigh levels of fat.Encapsulated rosemaryEOs showedbetter antimicrobial effect com-pared to standard rosemary EOs against L. monocytogenes in pork li-ver sausage; neither the direct effect of the level used nor mannerand effect of encapsulation are reported (Carraminana, Rota, Burillo,&Herrera, 2008). The activity of oreganoEOs againstClostridiumbot-ulinum spores in combination with low levels of sodium nitrite en-hanced the delay of growth of bacteria more than the sodiumnitrite alone, depending on the number of inoculated spores (Burt,2004). EOs extracted from the aerial parts of cultivated Salvia ofci-nalis L. were effective against Salmonella enteritidis (Hayouni et al.,2008). Winter savory (Satureja montana) EOs in combination withother preservation methods such as reduced temperature, pulsedlight, high pressure, pulsed electric and magnetic elds, irradiation,or packaging under a modied atmosphere can be utilized as eco-nomical natural antibacterial substance to control growth of food-borne bacteria and improve quality of minced pork (Carraminanaet al., 2008). Chinese cinnamon and winter savory EOs were usedsuccessfully to increase radio sensitivity in ground beef (Turgis,Borsa, Millette, Salimieri, & Lacroix, 2008). Combinations of EOsand nisin showed enhanced antimicrobial activities against L. mon-ocytogenes (Solomakos, Govaris, Koidis, & Botsoglou, 2008). Rancid-ity of heat-treated turkey-meat products was inhibited by aqueousextract of rosemary, sage and thyme (Mielnik, Sem, Egelandsdal, &Skrede, 2008). Treatments (homogenization) of meat with oreganoand sage EO signicantly reduced oxidation, while the heat treat-ment and storage time signicantly affected the antioxidant activityof the meat (Fasseas, Mountzouris, Tarantilis, Polissiou, & Zervas,2007).Milk protein-based edible lms containing oregano, pimento,or oregano/pimento were effective against Escherichia coli O157:H7or Pseudomonas sp. on meat surfaces (Mosqueda-Melgar et al.,2008a; Mosqueda-Melgar et al., 2008b; Oussalah et al., 2004).Chlorophyll-containing lms were tested against Staphylococcusaureusand Listeriamonocytogenes, showing that itwaspossible to re-duce growth of these micro-organisms inoculated in cooked frank-furters by covering the frankfurters with sodium magnesiumchlorophyllin-gelatin lms and coatings (Lpez-Carballo, Hernn-dez-Muoz, Gavara, & Ocio, 2008). Marjoram (Origanum majoranaL.) EOswere effective against several species of bacteria in fresh sau-sage (Busatta et al., 2008). Chlorophyllins are semi-synthetic por-phyrins obtained from chlorophyll. Chlorophyllin-gelatin lms andcoating applications successfully reduced Staphylococcus aureusand L. monocytogenes in cooked frankfurter (Lpez-Carballo et al.,2008). Individual extracts of clove, rosemary, cassia bark and liquo-rice demonstrated strong antimicrobial activity; but the mixture ofrosemary and liquorice extracts was the best inhibitor against allfour types ofmicrobes (L. monocytogenes, Escherichia coli, Pseudomo-nas uorescens and Lactobacillus sake) inmodied atmosphere-pack-

trol 21 (2010) 11991218aged fresh pork and vacuum-packaged ham slices stored at 4 C(Zhang, Kong, Xiong, & Sun, 2009). Santalum album, Cinnamomumcassia, andArtemisia capillariswere themost effective antimicrobials

Conin raw sheep meat (Luo et al., 2007). There are potential bio-preser-vative capabilities for applicationof clove and tea-tree oils to controlEscherichia coli O157:H7 on blanched spinach and minced cookedbeef (Moriera et al., 2007).

6.2. Fish

The high fat content of some sh, as with meat products, re-duces the antibacterial effect of EOs against various micro-organ-isms; however, some of the EOs had positive effects even in thehigh-fat-content shes. For example, oregano oil is more effectiveagainst the spoilage organism Photobacterium phosphoreum oncod llets than on salmon, which is a fatty sh. Oregano oil is moreeffective than mint oil in/on sh, even in fatty-sh dishes. Applica-tion of EOs on the surface of whole sh or as coating for shrimpsinhibited Salmonella Enteritidis, L. monocytogenes and naturalspoilage ora (Burt, 2004; Hayouni & Chraief et al., 2008).

There is signicant preservative and increased shelf-life effectsof wild thyme (Thymus serpyllum), about 15 to 20 days with fresh-water sh (Oral, Gulmez, Vatansever, & Guven, 2008). Strong anti-oxidant activity of oregano has been shown in a study by Goulasand Kontominas (2007). Shelf life of carp llets was extended four-fold by application of combined carvacrol + thymol with someother additives, compare to sterile 0.2% agar solution as a control(Mahmoud, Kawai, Yamazaki, Miyashita, & Suzuki, 2007). Antimi-crobial activity studies of garlic oil and nine compounds of EOsagainst bacterial isolates from carp showed that thymol, carvacroland cinnamaldehyde had the strongest antimicrobial activities, fol-lowed by isoeugenol, eugenol, garlic oil, and then citral for increas-ing the shelf life of carp llets, respectively (Mahmoud et al., 2004).Essential oils of Aloysia sellowii were successfully screened againsta variety of Gram-positive and -negative micro-organisms and twoyeasts in brine shrimp (Simionatto et al., 2005). The freshness indi-cator of tuna slices showed even better results after coating withan edible solution containing 0.5% eugenol plus 0.5% linalool, com-pared to controls (Abou-taleb & Kawai, 2008). Basil, clove, garlic,horseradish, marjoram, oregano, rosemary, and thyme have beenused successfully to implement hurdle technology for protectingseafood from the risk of Vibrio parahaemolyticus contamination(Yano et al., 2006). A synergistic effect of treatment with anodicelectrolyzed NaCl solution, combined with eugenol and linalool,has been found to enhance shelf-life extension of coated semi-friedtuna (Abou-taleb & Kawai, 2008).

6.3. Dairy products

It has been shown that extract ofmango seed kernel could reducetotal bacterial count, inhibit coliformgrowth, exert remarkable anti-microbial activity against an Escherichia coli strain and extend theshelf life of pasteurized cow milk (Abdalla et al., 2007). High wateractivity positively affects the application of EOs in milk by speedingthe transfer andmovementof EOs toward the targetedmicro-organ-isms (Cava, Nowak, Taboada, & Marin-Iniesta, 2007).

The antimicrobial activity of terpenes is not or is onlymarginallyinvolved in the explanation of the inuence of the botanical compo-sitionofmeadowson the sensoryproperties of pressed cheeses (Tor-nambeet al., 2008). Satureja cilicicaessential oil can serve inbutter asbothanatural antioxidantandaromaagent (Ozkan, Simsek,&Kulea-san, 2007). EOs from oregano, thyme, rosemary, sage, cumin andclove were tested on the growth of six bacteria, four of them usedas startersand twoof themas spoilage-causingbacteria (Viuda-Mar-tos et al., 2008). Cinnamon, cardamom and clove oils inhibit thegrowth of yoghurt starter cultures more than mint oil; however, in

M.M. Tajkarimi et al. / Foodother study mint oil was effective against Salmonella enteritidis inlow-fat yoghurt and cucumber salad (Burt, 2004). An in vitro studyon twelve ethanol extracts of propolis showed antimicrobial andantifungal activity especially at low levels against pathogenic mi-cro-organisms to protect starter culture strains in fermented prod-ucts (Kalogeropoulos, Konteles, Troullidou, Mourtzinos, &Karathanos, 2009). EOs of Melaleuca armillaris are effective againstlactic acid bacteria and may serve to improve the quality of foodproducts, depending on the LAB strain, as well as on the concentra-tion of the EOs (Hayouni, Bouix, Abedrabba, Leveau, & Hamdi,2008). EOs of clove, cinnamon, bay and thyme were tested againstL. monocytogenes and Salmonella enteritidis in soft cheese; clove oilwas found more effective against Salmonella enteritidis in full-fatcheese than in cheese slurry (Burt, 2004).

6.4. Vegetables

Application of antimicrobial activity of EOs in vegetables hasshown more successful results against natural spoilage ora andfood-borne pathogens in washing water, due to the low fat contentof the products. It can be enhanced by decreasing the pH of thefood and/or temperature. For example, oregano oil was effectiveagainst Escherichia coli O157:H7 and reduced nal populations ineggplant salad (Burt, 2004). Cinnamaldehyde and thymol wereeffective against six Salmonella serotypes on alfalfa seeds. Increas-ing temperature reduced the effectiveness of these antimicrobials,perhaps because of volatility decreasing permeability of the anti-bacterial compounds in the liquid media (Burt, 2004; Cava et al.,2007; Goni et al., 2009).

6.5. Rice

Leaves of ve different varieties of Ocimum basilicumwere effec-tive against three stored-rice pests (Sitophilus oryzae, Rhyzoperthadominica and Cryptolestes pusillus) (Lopez, Jordan, & Pascual-Vill-alobos, 2008). Sage oil and carvacrol were successfully used againstBacillus cereus in rice (Burt, 2004). Ocimum gratissimum and Thymusvulgaris have been used successfully against two major seed-bornefungi of rice in Cameroun (Nguefack et al., 2007).

6.6. Fruit

Natural ora on kiwi fruit (pH 3.23.6) was effectively inhibitedby carvacrol and cinnamaldehyde but less effectively on honeydewmelon (pH 5.45.5), which may result from the difference of pH be-tween the fruits (Burt, 2004). Natural fungicidal plant volatiles havebeen found more effective, compared to similar synthetic preserva-tives, against post-harvest fungal disease caused by Botrytis cinereain stored grapes (Tripathi et al., 2008). EOs incorporated into an algi-nate-based edible coating of fresh-cut Fuji apples showedmore than4-log reduction in the population of E. coli O157:H7. A total inhibi-tion of native microora for 30 days at 5 C, for preservation, taste,quality and pathogen control of the product has been shown. Themost effective antimicrobials were lemongrass and cinnamon EOs(0.7%, vol/vol), cinnamaldehyde (0.5%, vol/vol), and citral (0.5%,vol/vol) (Raybaudi, Rojas-Grau et al., 2008). Cinnamon, clove, andlemongrass EOs and their active compounds cinnamaldehyde, euge-nol, and citral have also shown promising antimicrobial and qualityeffects on fresh-cut melon (Raybaudi, Mosqueda-Melgar et al.,2008). Application of a combination of cinnamon and eugenol wastested for control of the germination of alicyclobacillus spores. Theapplication of 40 ppm cinnamaldehyde with 40 ppm of eugenol or80 ppm eugenol by itself preserved apple juice for 7 days (Bevilac-qua, Corbo, & Sinigglia, 2010). Polyphenols are present in green,white and commercial tea andare key antimicrobial and antioxidantcomponents for fresh-cut apple (Abou-taleb&Kawai, 2008). Combi-

trol 21 (2010) 11991218 1211nationof cinnamaldehydeandeugenolas anapple juicepreservativeagainst Alicyclobacillus acidoterrestris showed more acceptable re-sults in the test panels (Bevilacqua et al., 2010).

6.7. Animal feed

Application of thymol in animal feed shows effects on the bac-terial community in ani

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