Antimicrobial Herb

Food Control 21 (2010) 1199–1218

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Food Control

journal homepage: www.elsevier .com/locate / foodcont

Review

Antimicrobial herb and spice compounds in food

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

a Food Microbiology and Biotechnology Laboratory, North Carolina A&T State University, 171-B Carver Hall, Greensboro, NC 27411-1064, USAb Food Safety Laboratory, Department of Population Health and Reproduction, School of Veterinary Medicine, University of California, Davis One Shields Avenue, Davis,CA 95616-8743, USA

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

Article history:Received 9 December 2009Received in revised form 27 January 2010Accepted 2 February 2010

Keywords:Herbs and spicesNatural preservativesFood-borne pathogens

0956-7135/$ - see front matter � 2010 Elsevier Ltd. Adoi:10.1016/j.foodcont.2010.02.003

* Corresponding author. Tel.: +1 (336)334 7933; faE-mail address: [email protected] (M.M. Tajka

Herbs and spices containing essential oils (EOs) in the range of 0.05–0.1% have demonstrated activityagainst 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-microbial effects comparable to synthetic additives is still remote for three major reasons: limited dataabout their effects in food, strong odor, and high cost. Combinations of techniques have been successfullyapplied 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.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12002. Historical overview of plant antimicrobials . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12013. Major spice and herb antimicrobials. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1201

3.1. Chemical components present in EOs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1201
4. Uses of plant-origin antimicrobials . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1202
4.1. Mechanism of action. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12034.2. Synergistic and antagonistic effects of components . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1203

5. Review of some findings of in vitro experiments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1204
5.1. A. hydrophila . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12045.2. 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. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1210
6.1. Meat and poultry products . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12106.2. Fish. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12116.3. Dairy products . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12116.4. Vegetables . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12116.5. Rice. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12116.6. Fruit . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12116.7. Animal feed . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1212
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7. Effectiveness determinations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1212
7.1. Disc-diffusion method. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12147.2. Drop-agar-diffusion method . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12147.3. Broth microdilution method. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12147.4. Direct-contact technique in agar . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1214
8. Conclusions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1214References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1215

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 artifi-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 benefits (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, Fernández, & 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-Ryan, & Bourke, 2008b; Lopez-Malo vigil et al., 2005; Moriera,Ponce, Del Valle, & Roura, 2007; Patrignani et al., 2008; Periagoet al., 2006; Ponce et al., 2008; Raybaudi, Mosqueda-Melgaret al., 2008; Zaika, 1988). Even without a more comprehensiveunderstanding of how natural antimicrobial substances work,there is a growing effort to develop new effective methods that relyprimarily on their use to enhance food safety (Ayala-Zavala et al.,2008; Brandi et al., 2006; Chen et al., 2008; FAO/WHO Codex Ali-mentarius Commission., 2007; Liu, O’Conner, Cotter, Hill & Ross,2008; Lopez-Malo vigil et al., 2005; Martinez, Obeso, Rodriguez,& Garcia, 2008; Murdak et al., 2007; Nazef et al., 2008; Oussalah,Caillet, Salmiea, Saucier, & Lacroix, 2004; Pellegrini, 2003; Vaga-hasiya & Chanda, 2007).

In addition to their flavoring 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 fields for food preservation and con-trolling pathogens and spoilage micro-organisms in food. How-ever, technologies such as mild heat processing, modified-atmosphere packaging, vacuum packaging and refrigeration arenot sufficiently 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 ml�1(Burt, 2004).

For example, combined mild heat treatment with addition ofcinnamon and clove EOs to apple cider significantly reduced theD-value and time to 5-log reduction of Escherichia coli O157:H7(Knight & McKellar, 2007). Application of concentrations of 2.0%of citric acid or up to 0.1% of cinnamon bark oil in tomato juice, fol-lowed by treatment with high-intensity pulsed electric fields, suc-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 datapublished mostly in the past 10 years on plant-derived compoundsthat have been reported to be effective against spoilage or patho-genic bacteria, and practical methods for screening thesecompounds.

M.M. Tajkarimi et al. / Food Control 21 (2010) 1199–1218 1201

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 spices were used by the early Egyptians and have beenused for centuries in Asian countries such as China and India. Some ofthe spices, such as clove, cinnamon, mustard, garlic, ginger and mintare 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 flavorand aroma. Plant extracts and spices, in addition to contributing totaste and flavor, 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 first scientific 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 then other spices, such as allspice, bay leaf,caraway, coriander, cumin, oregano, rosemary, sage and thyme, havebeen reported to have significant bacteriostatic properties (Burt,2004; Ceylan & Fung, 2004; Gutierrez et al., 2008a; Jayaprakasha,Negi, Jena, & Jagan Mohan Rao, 2007; Kwon, Kwon, Kwon, & Lee,2008; Sofia, Prasad, Vijay, & Srivastava, 2007; Zaika, 1988).

Most 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 flavoring 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 flowers, 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, sage and van-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; Yoshida et al., 1999). Other spices, such as gin-ger, black pepper, red pepper, chili powder, cumin and curry powder,showed lower antimicrobial properties (Holley & Patel, 2005).

There are more than 1340 plants with defined 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 field and food systems. Food-preser-vative 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 quality

of 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 fluid 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-vation methods. 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 efficacy 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 flavonoids, thiosulfinates,glucosinolates and saponins.

Saponin and flavonoids are found in fruits, vegetables, nuts,seeds, stems, flowers, tea, wine, propolis and honey. They com-monly form a soapy lather after shaking in water. The antimicro-bial activity of saponins and flavonoids 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). Thiosulfinates 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 flavor 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,phenolic 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

Food 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, with more 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 offici-nale), galangal (Alpinia galanga), turmeric (Curcuma longa), and fin-gerroot (Boesenbergia pandurata) extracts against Gram-positiveand Gram-negative pathogenic bacteria at 0.2–0.4% (v/v) for finger-root and 8–10% (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 <10 and >30 mm by the disc-diffu-sion method (Agaoglu, Dostbil, & Alemdar, 2007).

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

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

Category Species Plant part

Herbs Basil, sweet (Ocimum basilicum) LeavesOregano (Origanum vulgare) Leaves/flowersRosemary (Rosmarinus offinicalis) LeavesSage (Salvia officinalis) 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/seed

Oils Olive oil FruitTea-tree oil (Melaleuca alternifolia) Leaves

genic and spoilage micro-organisms. Hydro-distilled EOs isolatedfrom the floral 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-ence 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 purified 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 the world, 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; Rodríguez 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 flavor component Bacterial inhibition (%)

Linalool/methyl chavicol <50Carvacrol/thymol 75–100Camphor/1,8-cineole/borneol/camphor 75–100Thujone, 1,8-cinole/borneol/camphor 50–75Thymol/carvacol 75–100

Eugenol/b-caryophyllene 75–100Cinnamic aldehyde/eugenol 75–100Eugenol 75–100Allyl isothiocyanate 50–75Myristicin/a-piene/Sabinene 50–75Vanillin (4-hydroxymethoxybenzaldehyde)/p-OH-benzyl methyl ether)

–

Oleuropein –Terpenoids –


4.1. Mechanism of action

It has been demonstrated that the antimicrobial effects of the EOsacts by causing structural and functional damages to the bacterialcell membrane. It is also indicated that the optimum range 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 0.05–0.1%(500–1000 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 modifications (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 significant 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 flagellin highly significantlyin 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 influence 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 benefit for nutritional and even more 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 significant effect on the EOs de-rived from Myrcia myrtifolia (De Cerqueira et al., 2007). The crudeextract of Sorghum bicolor Moench 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-skim milk, 10-fold in porkliver sausage, 50-fold in soup and 25–100-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 efficacy of plant-origin antimicrobials depends on factors such as the method ofextracting EOs from plant material, 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 Salmonella has been reducedby the effect of mustard’s EOs (Turgis et al., 2009).

Generally, Gram-negative bacteria are less sensitive to the anti-microbials 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 efficacy of EOsagainst pathogenic micro-organisms (Lambert, Skandamis, Coote,& Nychas, 2001).

Synergism between carvacrol and p-cymene, a very weak antimi-crobial, might facilitate carvacrol’s transportation into the cell bybetter swelling the B. cereus cell wall (Burt, 2004). Antimicrobialactivity of combination of cinnamon and clove EOs in vapor phaseshowed better antimicrobial with less active concentration in the va-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 Bacilluscereus was seen in rice when carvacrol and p-cymene were used withsalt; high-hydrostatic pressure showed a 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 2–3 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 inmodified-atmosphere packaging (MAP) including 40% CO2, 30% N2

and 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 from plant materi-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 findings 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 nisin with rosemary extractenhanced the bacteriostatic and bactericidal activity of the nisin(Thomas & Isak, 2006). Oregano EOs, in combination with modi-fied-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, 8–cine-ole (1:1) created more resistance in E. coli, compared to applicationof pure linalool. Either synergism or antagonism of 1, 8-cineoleand linalool derived from Cinnamosma fragrans could happen againstGram-negative bacteria and Fusarium oxysporu (Randrianariveloet al., 2009). The synergistic effect of different components could of-fer a way to prevent possible off flavor caused by clove and tea treewhen used to protect against Escherichia coli O157:H7 and minimize

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

Plant name Effective against Reference

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

Gram-positive and Gram-negative bacteria,including Listeria monocytogenes

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)

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

Bacillus subtilis, Clostridium botulinum,Escherichia coli, Listeria monocytogenes,Salmonella typhimurium and Staphylococcusaureus

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)

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

Pathogens such as Bacillus subtilis, Clostridiumbotulinum, Escherichia coli, Listeriamonocytogenes, Salmonella typhimurium,Staphylococcus aureus

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

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

Broad spectrum antibacterial effect againstGram-positive and Gram-negativepathogenic micro-organisms

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

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

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

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

Marjoram (Origanum majorana) Alternative for synthetic preservativesroutinely used in the food industry

Mahmoud et al. (2007)

Cumin (Cuminum cyminum) Bacillus cereus, Bacillus subtilis, Clostridiumbotulinum, Listena monocytogenes,Pseudomonas fluorescens, Salmonellaenteritidis, Staphylococcus aureus

Ceylan and Fung (2004)

Dill (Anethum graveolens) Clostridium botulinum, Pseudomonasaeruginosa, Staphylococcus aureus, Yersiniaenterocolitica


Fennel (Foeniculum vulgare) Bacillus cereus, Clostridium botulinum,Salmonella enteritidis, Staphylococcus aureus,Yersinia enterocolitica


Garlic (Allium vineale) Broad spectrum antibacterial effect againstGram-positive and Gram-negativepathogenic micro-organisms


Mint (Mentha piperita) Broad spectrum antibacterial effect againstGram-positive and Gram-negativepathogenic micro-organisms


Onion (Allium cepa) Escherichia coli, Salmonella typhimurium,Shigella dysenteriae, Staphylococcus aureus



off flavor effects in meat products (Moriera et al., 2007). Combina-tions of EOs of oregano and thyme, oregano with marjoram andthyme with sage had the most effects against Bacillus cereus, Pseudo-monas aeruginosa, Escherichia coli O157:H7 and L. monocytogenes(Gutierrez et al., 2008a).

5. Review of some findings 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 findings 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-

tracted 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 fluid 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 fischeri (Johnet al., 2008), EOs of the flower 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,

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 flavanols,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) films 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) films 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 films containingoregano, 1.0% (w/v), pimento, or 1.0% oregano pimento(1:1)], tannins, polymers of flavanols, 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 fluorescens Food spoilage Teas, [Milk protein-based edible films containingoregano, 1.0% (w/v) pimento, or 1.0% oreganopimento(1:1)], tannins, polymers of flavanols

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

Shigella spp. Tea Diarrhea Tea, Bersam engleriana(Melianthaceae), tannins,polymers of flavanols, 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)


Table 3 (continued)

Organism Adverseeffects

Inhibitors References

Salmonella spp. Foodpoisoning;Salmonellosis

Teas, leaf volatile oil; leaf oleoresin; eugenol; barkvolatile oil; bark oleoresin, E-cinnamaldehyde, [oreganoin whey protein isolate (WPI) films containing at 2%level, garlic essential oil at 3&4%], oregano (Origanumvulgare), and cinnamon (Cinnamomum zeylanicum),lemongrass, thyme (Thymus vulgaris), carvacrol,cinnamaldehyde, citral, and thymol), methanol extractof Aspilia mussambicensis (Compositae), Bersamaengleriana (Melianthaceae), Aristolochia indica L.,Brassica oleracea juice, dried garlic powder, commercialgarlic products, and garlic oil, marjoram and basilessential oils, cassia bark-derived substances,lemongrass, bay, methanol and acetone extracts of 14plants belonging to different families, thymol

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)

Spore forming bacteria Foodpoisoning

Catechins Friedman (2007)

Staphylococcus aureus Foodpoisoning;infection

Theasinensin, tea, cinnamon, oregano (Origanumvulgare), pure essential oils, leaf volatile oil, leaf oleoresin,eugenol, bark volatile oil, bark oleoresin, E-cinnamaldehyde, [oregano in whey protein isolate (WPI)films containing at 2% level, garlic essential oil at 3% and4%], dried garlic powder, commercial garlic products,clove, mustard, rosemary (Rosmarinus officinalis), lemonbalm (Melissa officinalis), sage (Salvia officinalis), chocolatemint (Mentha piperata), and oregano (Origanum vulgare),Bersama engleriana (Melianthaceae), chrysanthemumextracts, oil-macerated garlic extract, Petiveria alliacea L.root extract, Aristolochia indica L., tannins, polymers offlavanols, lemongrass and bay; certain combinations ofcarvacrol- thymol, citral, linalool and vapor, methanol andacetone extracts of 14 plants belonging to differentfamilies

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)

V. cholerae Cholera Tea extract Arques et al. (2008)

V. parahaemolyticus Mild gastro-enteritis

Basil, clove, garlic, horseradish, marjoram, oregano,rosemary, thyme, cassia bark-derived substances

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

Yersinia enterocolitica Diarrhea Teas, pure essential oils Friedman (2007), Lopez et al. (2007)

ToxinsBotulinum Neurotoxin

botulismBlack tea Friedman (2007)

Cholera Cholera Catechins, theaflavins Friedman (2007)

MoldsAspergillus flavus Myco-

toxicosisPure essential oils, leaf oleoresin, leaf volatile oil,eugenol, bark volatile oil, bark oleoresin, E-cinnamaldehyde, cassia bark-derived substances

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

Aspergillus niger Ochratoxins Methanol extract of Aspilia mussambicensis(Compositae)

Musyimi et al. (2008)

Aspergillus parasiticus Myco-toxicosis

Thymol Davidson and Naidu (2000)


Wang, Chen, & Fu, 2007), specific 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 0.1–1.0% 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 fischeri (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 (Sofia et al.,2007).

5.3. 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 minutiflorum with a capacity as a foodpreservative showed a variety of antimicrobial effects againstCampylobacter jejuni (Aslim & Yucel, 2007). The ciprofloxacinresistance of Campylobacter strains has been shown to bestrongly diminished by application of EO of Origanum minutiflo-rum (Aslim & Yucel, 2007).

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 modified-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 fillet,cubed

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

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

Salmon fillets Oregano oil Photobacterium phosphoreum No Burt (2004)Cod’s roe salad Mint oil Salmonella enteritidis Yes (+++) Burt (2004)

Coated semi-friedtuna slices

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

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

Yes Oral et al. (2008)

Lightly saltedcultured seabream (Sparusaurata) fillets

Oregano Increased shelf life, antioxidantactivity

Yes Goulas and Kontominas (2007)

Carp fillets 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 g�1(+) Burt (2004)

(continued on next page)


Table 4 (continued)

Food group EO or component Bacterial species Inhibitory effect Reference

Yoghurt Clove, cinnamon, cardamom, peppermintoil

Streptococcus thermophilus Yes (Mint oil +,Cardamom, clove:++, Cinamon:+++)

Burt (2004)

Tzatziki (yogurt andcucumber salad)

Mint oil Salmonella enteritidis From 1.5%v/w ++ Burt (2004)

Butter Satureja cilicica essential oil Antioxidant Yes Ozkan et al. (2007)

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

Starter cultures and related foodspoilage

Yes Viuda-Martos et al. (2008)

VegetablesLettuce, romaine Thyme oil E. coli O157:H7 Yes (+) Burt (2004)

Carrots Thyme oil E. coli O157:H7 Yes (+�++) Burt (2004)

Lettuce, iceberggreen

Basil methyl chaviol (BMC) Natural flora Yes (++) Burt (2004)

Eggplant salad Oregano oil E. coli O157:H7 Yes (++) Burt (2004)

Alfalfa seeds Cinnamaldehyde, thymol Salmonella spp., six serotypes Yes (50 �C: +, 70 �C:0)

Burt (2004)

RiceBoiled rice Carvacrol Natural flora Yes (+++) Burt (2004)

Boiled rice Sage oil Bacillus cereus, Staphylococcusaureus, Salmonella typhimurium

No Burt (2004)

Rice Ocimum basilicum Three stored-rice pests(Sitophilus oryzae, Rhyzoperthadominica and Cryptolestespusillus)

Yes Lopez et al. (2008)

FruitKiwifruit Carvacrol, cinnamic acid Natural flora Yes (+++) Burt (2004)

Honeydew melon Carvacrol, cinnamic acid Natural flora Yes (0�+) Burt (2004)


5.4. 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 flowers of Salviareuterana (Lamiaceae) (Esmaeili et al., 2008), linalool vapor of ber-gamot and linalool oils (Fisher & Phillips, 2008),water-distilled EOfrom leaves and flowers of Micromeria nubigena H.B.K. (Lamiaceae)(El-Seedi et al., 2008), hydro distillation leaf oil of Cinnamomumchemungianum (Raj et al., 2008), Rosmarinus officinalis 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 0.12–0.25% 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 flower 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 (Sofia et al., 2007).

5.6. L. monocytogenes

Rosmarinus officinalis 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 0.5–0.7 w/v and were bacte-riostatic at 0.5–1.0% concentration; and borneol extracted fromsage and rosemary had inhibitory effect against L. monocytogenesat 0.02–0.05% 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. flavus; 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 flowers of Microm-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 Aflatoxins productionhas been inhibited by Thymus vulgari and Citrus aurantifolia,whereas Mentha spicata L., Foeniculum miller, Azadirachta indica A.


Juss, Conium maculatum and Artemisia dracunculus has only inhib-ited the fungal growth, while Carum carvi L. has controlled afla-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 flower-ing stages) and flowers 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-grass, have been more effective as volatiles (Suhr & Nielsen,2003); 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, specifically 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 flowers 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 fisc-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-terial species such as Pseudomonas fluorescens (Raj et al., 2008).Guarana extract (Majhenic et al., 2007) and leaves, bark and fruitsof Neolitsea fischeri (John et al., 2008) were active against Pseudo-monas fluorescens.

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 flavoring, Zataria multiflora 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 0.12–0.25% v/vconcentration (Davidson & Naidu, 2000), leaves bark and fruits ofNeolitsea fischeri (John et al., 2008, hydro-distilled EOs of freshleaves and mature fruits of Pittosporum viridulum (John et al.,2007).

According to a study on Mueller–Hinton (MH) Agar and MHbroth, cloves showed antimicrobial effect against Shigella sonnei,Shigella flexneri 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 flowers 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 officinalis oil (Gachkar et al., 2007); EOs ofZataria multiflora 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 0.4–0.6% 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 175–225 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 0.12–0.25% 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 fisc-heri (John et al., 2008), water-distilled EOs from leaves and flowersof Micromeria nubigena H.B.K. (Lamiaceae) (El-Seedi et al., 2008),Curcuma domestica and Curcuma viridiflora at ratios of 20/15 (Chenet al., 2008), anzer tea’s EOs (Sekeroglu et al., 2007), EOs of theflower 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 flavanols (Yilmaz, 2006), and Curcumadomestica and Curcuma viridiflora 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 flowering stages) and flow-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-positivebacteria (Bajpai et al., 2008). Linalool and methyl chavicol vanillinextracted from sweet basil vanilla showed inhibitory effect against33–35 bacteria, yeasts and molds (Davidson & Naidu, 2000).


Bergamot peel (Mandalari et al., 2007) is effective against gram-negative bacteria. Origanum oil, extracted by steam distillation 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 effluent, can prevent coliform re-growth for up to 14 days(Winward, Avery, Stephenson, & Jefferson, 2008). Antimicrobialactivity of EOs extracted from Thymus vulgaris (thymol chemotype),Thymus zygis subsp. gracilis (thymol and two linalool chemotypes)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 to1.25–5 mg/ml for Gram-negatives (Oleszek, 2000). MIC of oreganoEOs were lower than thyme and cinnamon EOs, against Gram-nega-tive pathogenic micro-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 flavus) (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 floral 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 (Sofia 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.Finding the most inhibitory spices and herbs depends on a numberof 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-ity 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, the

same 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 flora in meat products. However, mus-tard, cilantro, mint and sage oils were less effective or ineffective(Burt, 2004). A 5–20 ll g�1 level of eugenol and coriander, clove,oregano and thyme oil inhibits growth of L. monocytogenes, Aeromo-nas hydrophila and autochthonous spoilage flora 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 in meat products can be reduced by high levels of fat.Encapsulated rosemary EOs showed better 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 oregano EOs against Clostridium bot-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 offici-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 fields, irradiation,or packaging under a modified 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 significantly reduced oxidation, while the heat treat-ment and storage time significantly affected the antioxidant activityof the meat (Fasseas, Mountzouris, Tarantilis, Polissiou, & Zervas,2007). Milk protein-based edible films 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 films were tested against Staphylococcusaureus and Listeria monocytogenes, showing that it was possible to re-duce growth of these micro-organisms inoculated in cooked frank-furters by covering the frankfurters with sodium magnesiumchlorophyllin-gelatin films and coatings (López-Carballo, Hernán-dez-Muñoz, Gavara, & Ocio, 2008). Marjoram (Origanum majoranaL.) EOs were 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 films andcoating applications successfully reduced Staphylococcus aureusand L. monocytogenes in cooked frankfurter (López-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 of microbes (L. monocytogenes, Escherichia coli, Pseudomo-nas fluorescens and Lactobacillus sake) in modified atmosphere-pack-aged fresh pork and vacuum-packaged ham slices stored at 4 �C(Zhang, Kong, Xiong, & Sun, 2009). Santalum album, Cinnamomumcassia, and Artemisia capillaris were the most effective antimicrobials


in raw sheep meat (Luo et al., 2007). There are potential bio-preser-vative capabilities for application of 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 fish, 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 fishes. For example, oregano oil is more effectiveagainst the spoilage organism Photobacterium phosphoreum oncod fillets than on salmon, which is a fatty fish. Oregano oil is moreeffective than mint oil in/on fish, even in fatty-fish dishes. Applica-tion of EOs on the surface of whole fish or as coating for shrimpsinhibited Salmonella Enteritidis, L. monocytogenes and naturalspoilage flora (Burt, 2004; Hayouni & Chraief et al., 2008).

There is significant preservative and increased shelf-life effectsof wild thyme (Thymus serpyllum), about 15 to 20 days with fresh-water fish (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 fillets 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 fillets, 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 of mango seed kernel could reducetotal bacterial count, inhibit coliform growth, 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 and movement of EOs toward the targeted micro-organ-isms (Cava, Nowak, Taboada, & Marin-Iniesta, 2007).

The antimicrobial activity of terpenes is not or is only marginallyinvolved in the explanation of the influence of the botanical compo-sition of meadows on the sensory properties of pressed cheeses (Tor-nambe et al., 2008). Satureja cilicica essential oil can serve in butter asboth a natural antioxidant and aroma agent (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 starters and two of them as spoilage-causing bacteria (Viuda-Mar-tos et al., 2008). Cinnamon, cardamom and clove oils inhibit thegrowth of yoghurt starter cultures more than mint oil; however, inother 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 and

antifungal 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 flora 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 final 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 five different varieties of Ocimum basilicum were 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 flora on kiwi fruit (pH 3.2–3.6) was effectively inhibitedby carvacrol and cinnamaldehyde but less effectively on honeydewmelon (pH 5.4–5.5), 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 showed more than4-log reduction in the population of E. coli O157:H7. A total inhibi-tion of native microflora 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 and are key antimicrobial and antioxidantcomponents for fresh-cut apple (Abou-taleb & Kawai, 2008). Combi-nation of cinnamaldehyde and eugenol as an apple juice preservativeagainst 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 animal feed (Janczyk, Trevisi, Souffrant, & Bosi,2008). EO compounds showed limited effects on nutrient utiliza-tion in studies of alfalfa silage and corn silage as the sole foragesource in ruminants (Benchaar et al., 2007). Effects of cinnamonleaf oil on total volatile fatty acid (VFA) concentration have beenstudied. It was concluded that it inhibits propionate-producingbacteria and might have an adverse effect on metabolism and pro-ductivity of ruminants (Fisher & Phillips, 2008).

Table 5Different screening methods for evaluating activity of plant-origin antimicrobials against d10 years.

Food-borne pathogen Method

Bacillus cereus, Pseudomonas aeruginosa andEscherichia coli

Adjusted suspensions of micro-orproper agar and solidify the mixtudiscs were inserted into the platesolution of each extract were tranincubated at proper temperature

Escherichia coli and Staphylococcus aureus Direct contact assay method in orInhibitory Concentration (MIC).

Escherichia coli and Staphylococcus aureus Modified disc-diffusion method orTurnidge, and Washington (1995)

Bacillus cereus Luria–Bertani (LB) agar plates

Bacillus cereus, Escherichia coli O157:H7, Listeriamonocytogenes and Salmonella enterica

The modified bactericidal assay dFriedman, Henika, Levin, Mandrel

Escherichia coli and Pseudomonas fluorescens Well-diffusion test described by K(1995)

Gram-negative, Gram-positive bacteria and molds Modified vapor diffusion test whiby Isidorov and Vinogorova (2005

Escherichia coli, Bacillus cereus and Pseudomonasfluorescens

Method described by Janssen, SchSvendsen (1987) and Vagi, Siman(2005)

Bacillus cereus, Pseudomonas aeruginosa andEscherichia coli

Pit and disc methods according toTowers (2002)

Campylobacter jejuni Different concentrations of mainderived cinnamon and oregano oibuffered saline

Escherichia coli Modified method explained by FrMandrell (2002), Friedman, Henik(2004)

Bacillus cereus, Bacillus subtilis Staphylococcusaureus, Escherichia coli, Salmonella typhi andPseudomonas aeruginosa

Growth zone-inhibition developeDavidson and Parish (1989)

Salmonella enteritidis, Escherichia coli O157:H7,Listeria monocytogenes and Staphylococcusaureus

Zone of inhibition assay on solid

Escherichia coli, Staphylococcus aureus and Bacilluscereus

Disc-diffusion technique

Escherichia coli Agar plate method

Salmonella typhimurium, Pseudomonas aeruginosa,Escherichia coli, Staphylococcus aureus, Bacilluscereus, Bacillus subtilis and Salmonellatyphimurium

Agar disc-diffusion method (Nair,2005)

Vibrio parahaemolyticus and Escherichia coli Screening growth or survival of thdifferent temperatures in nutriendefined pH

7. Effectiveness determinations

Comparison of published data regarding different methods iscomplicated: according to some investigators there is increased var-iation based on extraction method, culture medium, size of inocu-lum, choice of emulsifier and basic test method (Sofia et al., 2007).Antimicrobial activity in most experiments has been quantified ontwo bases, MIC and MBC (minimum bactericidal concentration),which is presumably greater than the MIC. MIC is defined in differentterms; some of them are ‘‘lowest concentration resulting in mainte-nance or reduction of inoculum’s viability,” ‘‘lowest concentration

ifferent food-borne pathogenic micro-organisms – studies conducted within the last

Inhibitors Reference

ganisms were placed inre in Petri plates, sterile

s. And proper volumesferred to the discs andand time

Catechins Arques et al.(2008)

der to define Minimum Cinnamon or oregano Becerril et al.(2007)

iginated from Jorgensen, Four strains of TunisianChrysanthemum species

Ben Sassi et al.(2008)

Tea flavonoids Friedman(2007)

escribed previously byl, Kozukue (2006)

Extract of oregano leaves with addedgarlic juice and oregano oil

Friedman,Henika, Levin,& Mandrell(2007)

im, Marshall et al. Different ethanol extracts of soiceshoneysuckle, Scutellaria, Forsythiasuspensa (Thunb), cinnamon,rosemary and clove oil

Kong et al.(2007)

ch is explained in detail)

Three commercially availableessential oils (EOs) cinnamon ,thyme,and oregano

Lopez et al.(2007)

effer, and Baerheimdi, Suhajda, and Hethelyi

Guarana seed extract Majhenic et al.(2007)

Rajakanuna, Harris, and Methanol extract of Aspiliamossambicensis (Compositae)

Musyimi et al.(2008)

constituents of plant-ls, in sterile phosphate-

Cinnamaldehyde and carvacrol Ravishankaret al. (2008)

iedman, Henika, anda, Levin, and Mandrell

Oregano oil/carvacrol; cinnamon oil/cinnamaldehyde; and lemongrass oil/citral

Rojas-Grauet al. (2007)

d method described by Volatile oils and oleoresin ofCinnamomum zeylanicum Blume(leaf and bark)

Singh et al.(2007)

medium Oregano, rosemary and garlicessential oils

Seydim andSarikus (2006)

Six Indian spice extracts: clove,cinnamon, mustard, garlic, ginger andmint

Winward et al.(2008)

Cabbage juices Tolonen et al.(2004)

Kalariya, & Chanda, Methanol and acetone extracts of 14plants belonging to different families

Vagahasiyaand Chanda(2007)

ese two bacteria att-rich medium and

18 Plant species Yano et al.(2006)


required for complete inhibition of test organism up to 48 h incuba-tion,” ‘‘lowest concentration inhibiting visible growth of test organ-ism,” or ‘‘lowest concentration resulting in a significant decrease ininoculum’s viability (>90%).” MBC is defined as ‘‘concentrationwhere 99.9% or more of the initial inoculum is killed” or ‘‘lowest con-centration at which no growth is observed after sub-culturing intofresh broth.” The MIC method is cited by most researchers, but somequote MBC as a measure of antibacterial performance (Brandi et al.,2006; Romeo et al., 2008). MICs for carvacrol, thymol, eugenol, per-illaldehyde, cinnamaldehyde and cinnamic acid were in the range of0.05–5 ll m�1 in vitro (Burt, 2004). The in vitro EO studies using agarto determine MICs are generally are the same order of magnitude.The optical density (OD) (turbidity) measurement and the enumer-ation of colonies by viable count are the most-used methods. Theredox indicator resazurin has been used recently in a new microdilu-tion method (Burt, 2004). New approaches and advances inextraction methods, such as crude extraction, high-intensity ultra-sound-assisted (HI-US) in combination with proper solvent selec-tion, can improve these approaches (Burt, 2004; Ibrahim, Tse,Yang, & Fraser, 2009; Romeo et al., 2008; Thongson, Davidson, Maha-karnchanakul, & Weiss, 2004). Thirty-eight strains of Salmonellahave been tested with some modifications in the diffusion techniqueto evaluate antimicrobial activity of chive extract (Ibrahim et al.,2009). The most-used methods for quantitative and qualitative eval-uation of EOs of plants and spices are in vitro or exploratory (end-point and descriptive methods) and applied (inhibition curves andendpoint methods). Diffusion, dilution or bio-autographic methodsare categories of antimicrobial activity tests (Brandi et al., 2006).However, there are some observed anomalies in screening of antimi-crobial activity against Staphylococcus aureus, with a greater reduc-tion of growth at the MIC than at the MBC (Becerril et al., 2007).Moreover, there are differences among publications between defini-

Table 6Antibacterial activity of various concentrations of spices, as a function of the screening m

Spice Concentration (%)b Bacillus cereus

Discc Well/cupd

Cinnamon 0.5 10.3 ± 0.5 –1 11.0 ± 0.0 10 ± 02 11.3 ± 0.5 11.6 ± 0.53 12.0 ± 0.0 13.3 ± 0.5

Clove 0.5 10.3 ± 0.5 –1 11.3 ± 0.5 14.6 ± 0.52 12.6 ± 0.5 23.6 ± 0.53 16.0 ± 0.0 25.6 ± 0.5

Garlic 0.5 11.6 ± 0.5 –1 12.6 ± 0.5 –2 14.0 ± 0.0 –3 14.3 ± 0.5 10.6 ± 0.5

Ginger 0.5 9.6 ± 0.5 –1 10.3 ± 0.5 –2 11.0 ± 0.0 10.3 ± 0.53 11.6 ± 0.5 11.3 ± 0.0

Mint 0.5 11.3 ± 0.5 13.3 ± 0.51 14.6 ± 1.1 14.0 ± 0.02 14.6e ± 0.5 14.6e ± 0.53 18.3e ± 1.1 16.6e ± 0.5

Mustard 0.5 – –1 10.3 ± 0.5 9.6 ± 0.52 11.6 ± 0.5 10.3 ± 0.53 15.6 ± 0.5 11.3 ± 0.5

Differences between different concentrations within a spice found to be significant at PAdapted from Winward et al. (2008).

a All readings are mean of triplicates ± SD, in mm diameter.b All controls (0% spice) showed negligible inhibition.c Diffusion from paper disc on inoculated agar.d Diffusion from cup or well into inoculated agar.e Unclear zones of inhibition.

tions and among procedures used in preparation of the tested sam-ples (Brandi et al., 2006; Burt et al., 2007; Kim et al., 2006). Methodssuch as solvent-free microwave extraction (SFME) and application ofcrude extracts and enzyme conversions of herbs and spices will im-prove efficacy and extraction rates, with shorter extraction timesand higher levels of active antimicrobial components. Crude extractsof herbs and plants have demonstrated oxidative degradation andantioxidant properties (Bendahou et al., 2008; Ibrahim et al., 2009;Kahkonen et al., 1999; Mandalari et al., 2007). In SFME method, amicrowave is used and a plant material is inserted into an extractionvessel with hexane, more detailed information is provided in Benda-hou et al. (2008). Vapor-phase experiments are more reliable meth-ods in determining antimicrobial properties; in this method theconcentration is expressed as weight per unit volume (mg/l air),and the sterile blank filter disc is placed in the center of the lid ofthe Petri dish (Goni et al., 2009).

The disc-agar-diffusion method, drop-agar diffusion methodand direct-contact technique in agar are the usual techniques inthe screening approach, which has been described in detail in otherreferences (Burt, 2004).

Identification of antimicrobial activity is significantly affected bythe method of assay and may be interfered with by various food com-ponents and/or addition of compounds such as bovine serum albu-min (BSA) (Burt, 2004; Davidson & Naidu, 2000). High-pressureextraction (with pure CO2 and with co-solvent) was more effectivemethod than low pressure to obtain extracts (Kitzberger et al.,2007). Other techniques in antimicrobial determination are: dilu-tion of the EO in agar or broth which showed similar approaches be-tween methods and definitions, broth-dilution studies withbacterial enumeration by optical density (OD) (turbidity) measure-ment, and application of the redox indicator resazurin as a visualindicator of the MIC (Brandi et al., 2006; Holley & Patel, 2005). Table 5

ethod.a

Escherichia coli Staphylococcus aureus

Disc Well/cup Disc Well/cup

8.0 ± 0.0 – – –10.0 ± 0.0 10.6 ± 0.5 – 10 ± 012.3 ± 0.5 12.6 ± 0.5 10.0 ± 0.0 10.6 ± 0.514.3 ± 0.5 14 ± 1 11.6 ± 0.5 12.3 ± 0.5

11.6 ± 0.5 16.3 ± 0.5 – –13.3 ± 0.5 17.3 ± 0.5 – 18.3 ± 0.515.6 ± 0.5 20.3 ± 0.5 12.6 ± 0.5 23.6 ± 0.519.3 ± 0.5 23.3 ± 0.5 16.3 ± 0.5 25.6 ± 0.5

10.0 ± 1.0 10.3 ± 0.5 10.6 ± 0.5 –10.0 ± 0.0 12.3 ± 0.5 12.0 ± 0.0 –11.3 ± 0.5 13.0 ± 1.0 12.3 ± 0.5 10.3 ± 0.512.3 ± 0.5 13.0 ± 0.0 14.0 ± 1.0 11.6 ± 0.5

9.3 ± 0.5 – 10.6 ± 1.1 –10.3 ± 0.5 – 11.3 ± 0.5 –10.6 ± 0.5 10.0 ± 0.0 13.0 ± 1.0 10.6 ± 0.5

11.3e ± 0.5 11.3 ± 0.5 14.6 ± 0.5 12.3 ± 0.5

– – 12.6 ± 0.5 13.3 ± 0.513.3 ± 0.5 – 14.3 ± 0.5 14.6 ± 0.5

15.0e ± 1.0 8.6e ± 0.5 15.0e ± 1.0 26.6e ± 0.516.3e ± 0.5 9.3e ± 0.5 17.3e ± 0.5 27.6e ± 0.5

11.6 ± 0.5 8 ± 0 10.3 ± 0.5 –19.3 ± 0.5 12.6 ± 0.5 11.6 ± 0.5 –21.6 ± 0.5 14.6 ± 0.5 14.3 ± 0.5 8.3 ± 0.525.6 ± 0.5 19.3 ± 0.5 16.0 ± 1.0 9.6 ± 0.5

< 0.05.


demonstrates some different screening methods for evaluating theantimicrobial activity of different plant-origin antimicrobialsagainst different food-borne pathogenic micro-organisms.

7.1. Disc-diffusion method

The Food and Drug Administration (FDA) has been approved thismethod as a standard for the National Committee for Clinical Labo-ratory Standards (Turker & Usta, 2008). The disc-diffusion methodis the most often-used technical method for antimicrobial screen-ings of EOs. Antimicrobial activity is generally evaluated by thismethod for preliminary studies. In this method, a paper disc soakedwith the EO is placed on the inoculated surface of an agar plate andthe zone of microbial inhibition is measured. Different parametersin this test could affect the result, such as the volume of EO on the pa-per discs, the thickness of the agar layer and the solvent. For exam-ple, some of reported solvents are ethanol, methanol, Tween-20,Tween-80, acetone in combination with Tween-80, polyethyleneglycol, propylene glycol, n-hexane and dimethyl sulfoxide, whichcould result in difficulties when comparing different studies (Brandiet al., 2006; Burt et al., 2007). More precise data regarding extractantimicrobial evaluation have been obtained with this method (Kilet al., 2009). Table 6 shows antimicrobial activities against Esche-richia coli, Bacillus cereus, and Staphylococcus aureus measured bythe paper disc-diffusion technique and well or cup method.

7.2. Drop-agar-diffusion method

The drop-agar-diffusion method has been described in detail(Cruz et al., 2007; Hammer, Carson, & Riley, 1999; Hili, Evans, & Ve-ness, 1997). The inhibition zones of EOs against food-borne andother pathogens have been measured by this method (Saif Mokbel& Suganuma, 2006). This was the method used for testing antimi-crobial activity of extracts from aerial parts of seven wild sagesfrom Western Canada – Artemisia absinthium L., Artemisia biennisWilld, Artemisia cana Pursh, Artemisia dracunculus L., Artemisia frig-ida Wlld, Artemisia longifolia Nutt. and Artemisia ludoviciana Nutt. –against bacteria, yeasts and fungi, including Escherichia coli, Staph-ylococcus aureus, Candida albicans and Aspergillus niger (Lopes-Lutzet al., 2008).

7.3. Broth microdilution method

The broth microdilution method was used for antimicrobialactivity evaluation of aerial parts of fresh Plectranthus cylindraceusoil against Staphylococcus aureus and Bacillus subtilis (Mohsen-zadeh, 2007). According to Davidson and Naidu (2000), this meth-od showed lower MICs (% v/v) of different essential oils extractedfrom bay, clove, peppermint and thyme against Escherichia coli,Staphylococcus aureus and Candida albicans, compared to agar-dilu-tion assay. This method was used by Radusiene et al. (2007) toevaluate the antimicrobial activity of Acorus calamus against 17species of bacteria, yeasts and fungi.

7.4. Direct-contact technique in agar

The direct-contact technique in agar has been used for screeningthe antimicrobial activity of carvacrol, the EO produced from Thymusciliatus sp. eu-ciliatus, against Staphylococcus aureus and Escherichiacoli (Bousmaha-Marroki, Atik-Bekkara, Tomi, & Casanova, 2007).

8. Conclusions

Plant-origin antimicrobials are present in a variety of plants,spices and herbs. Spices and herbs are used for both flavoring

and preservation purposes. Spices and herbs, which were originallyadded for improving taste, can also naturally and safely improveshelf life of food products (Holley & Patel, 2005).

There are a variety of methods for testing the antimicrobialactivities of spices, herbs and their components. These methodsstrongly affect the observed level of inhibition; there is a differencein activity against micro-organisms between each individual andor combination of spices and herbs. Various reasons may contrib-ute in the differences between results, including inconsistency be-tween analyzed plant materials even in the same leaves (Radusieneet al., 2007). The low pH level might work as a result of direct effectof the pH or the effect on EOs on the lipid phase of the bacterialmembrane (Abou-taleb, & Kawai, 2008; Akhondzadeh Basti et al.,2007). Organoleptic and safety issues in application of the EOs infood must be addressed. Application of traditional and naturalantimicrobials has been recently outlined by regulatory agenciesin the US. Based on Code of Federal Regulation 21 CFR part182.20, EOs of cinnamon, clove, lemon grass and their respectiveactive compounds (cinnamaldehyde, eugenol and citral, respec-tively) are generally recognized as safe (GRAS) (Raybaudi, Rojas-Grau et al., 2008; Turgis et al., 2009). Application of Vapor phasecombination of Eos showed successful results for an antimicrobialpackaging development with less active components of cinnamonand clove (Goni et al., 2009).

Changes in flavor due to application of antimicrobial compo-nents are a major issue. However, flavor has not been affected afterapplication of eugenol oil (Eugenia caryophylata) against four applepathogens in fresh-cut apple (Amiri et al., 2008). Application ofedible and bio-base films with different EOs in the packaging pro-cess of sausage casing and processed cheese slices will need furtherinvestigation (Seydim & Sarikus, 2006). However, some materials,such as thymol, have not been recognized as food-grade additivesby European legislation (Falcone, Speranza, Del Nonile, Corbo, &Sinigaglia, 2005).

In the EU countries, EOs as flavorings have been registered andrecognized as safe-to-use materials: carvacrol, carvone, cinnamal-dehyde, citral, p-cymene, eugenol, limonene, menthol and thymolare in this group; however, two EO components, estragole andmethyl eugenol, have been deleted from the safe list in 2001.Application of whole EOs seems to be more feasible for most coun-tries, due to the costs of procedures to evaluate safety of any addedflavoring materials (Burt, 2004). Synergism and antagonism ofthese materials need to be further investigated before their broadapplication in the food industry. It is necessary to define a targetand effective range for each EO, including MIC and safety data (tox-icity, allergenicity) in food materials (Svoboda et al., 2006).

Application of plant-origin antimicrobials needs to be addressedby regulatory authorities for most parts of these compounds.Assessment of the effect of high doses of some EOs on intestinalcells, as well as cost and odors created by high concentrations ofthese materials, also should be considered seriously. Several suc-cessful combined methods of application of these EOs in conjunc-tion with new approaches such as hurdle technology andmodified-atmosphere packaging created pleasant odor with longershelf life (Burt, 2004; Davidson, 2006; Fisher & Phillips, 2008;Friedman, 2007; Goulas & Kontominas, 2007; Naidu, 2000a; Proes-tos et al., 2008; Silva et al., 2007). According to Lanciotti et al.(2004), other possible ways to reduce the organoleptic impactinclude:

(1) Minimizing perception of the presence of spices/herbs andEOs in food by optimizing food formulation.

(2) Application of combined methods.(3) Enhancing a calibrated vapor pressure capacity in order to

increase interaction between EO and the bacterial cellmembrane.


Evaluation of new preservatives such as natural antimicrobialsin food, evaluating food structure, composition and interaction be-tween natural microflora and food-borne disease agents could bemade much more precise by application of predictive models(Koutsoumanis et al., 1999).

Several studies have been focused on the application of individ-ual EOs derived from plants. Some studies showed whole EOs havemore antimicrobial activity compared to the mixture of majorcomponents (Burt, 2004). However, information on the effects ofthese natural compounds in combination and or as crude extractsagainst food-borne micro-organisms is limited (Ibrahim et al.,2009; Mandalari et al., 2007).

The future will see much-needed investigation of food applica-tions of the naturally occurring antimicrobials, especially the effec-tiveness of EOs, individually and in combination with other parts ofplant extract, other effective EOs and other food-processingtechniques.

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