Antiamoeba

Food Control 21 (2010) 11991218
Contents lists available at ScienceDirect
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
Food Microbiology and Biotechnology Laboratory, North Carolina A&T State University, 171-B Carver Hall, Greensboro, NC 27411-1064, USA 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
b a
a r t i c l e
i n f o
a b s t r a c t
Herbs and spices containing essential oils (EOs) in the range of 0.050.1% have demonstrated activity against pathogens, such as Salmonella typhimurium, Escherichia coli O157:H7, Listeria monocytogenes, Bacillus cereus and Staphylococcus aureus, in food systems. Application of herbs, spices and EOs with antimicrobial effects comparable to synthetic additives is still remote for three major reasons: limited data about their effects in food, strong odor, and high cost. Combinations of techniques have been successfully applied in several in-food and in vitro experiments. This paper aims to review recent in-food applications of EOs and plant-origin natural antimicrobials and recent techniques for screening such compounds. 2010 Elsevier Ltd. All rights reserved.
Article history: Received 9 December 2009 Received in revised form 27 January 2010 Accepted 2 February 2010
Keywords: Herbs and spices Natural preservatives Food-borne pathogens
Contents 1. 2. 3. 4. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Historical overview of plant antimicrobials . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Major spice and herb antimicrobials. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1. Chemical components present in EOs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Uses of plant-origin antimicrobials . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1. Mechanism of action . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2. Synergistic and antagonistic effects of components . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Review of some findings of in vitro experiments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.1. A. hydrophila . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.2. Bacillus sp. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.3. C. jejuni . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.4. Clostridium perfringens . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.5. Escherichia coli . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.6. L. monocytogenes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.7. Molds and yeasts. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.8. Pseudomonas sp. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.9. Salmonella sp. and Shigella sp. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.10. Staphylococcus aureus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.11. Vibrio parahaemolyticus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.12. General Gram-positive and Gram-negative bacteria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Some in-food experiments with plant-origin antimicrobials. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.1. Meat and poultry products . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.2. Fish. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.3. Dairy products . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Vegetables . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.4. 6.5. Rice. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.6. Fruit . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.7. Animal feed . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1200 1201 1201 1201 1202 1203 1203 1204 1204 1204 1206 1208 1208 1208 1208 1209 1209 1209 1209 1209 1210 1210 1211 1211 1211 1211 1211 1212
5.
6.
* Corresponding author. Tel.: +1 (336)334 7933; fax: +1 (336)334 7239. E-mail address: Tajkarimi@gmail.com (M.M. Tajkarimi). 0956-7135/$ - see front matter 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.foodcont.2010.02.003
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M.M. Tajkarimi et al. / Food Control 21 (2010) 11991218
7.
8.
Effectiveness determinations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.1. Disc-diffusion method. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.2. Drop-agar-diffusion method . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.3. Broth microdilution method . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.4. Direct-contact technique in agar . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Conclusions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
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1. Introduction Strong consumer demand for safe and high-quality foods can be attributed in part to the widespread availability and accessibility of quality health data and information. There are also new concerns about food safety due to increasing occurrence of new food-borne disease outbreaks caused by pathogenic micro-organisms. This raises considerable challenges, particularly since there is increasing unease regarding the use of chemical preservatives and articial antimicrobials to inactivate or inhibit growth of spoilage and pathogenic 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 a consequence, natural antimicrobials are receiving a good deal of attention for a number of micro-organism-control issues. Reducing the need for antibiotics, controlling microbial contamination in food, improving shelf-life extension technologies to eliminate undesirable pathogens and/or delay microbial spoilage, decreasing the development of antibiotic resistance by pathogenic microorganisms or strengthening immune cells in humans are some of the benets (Abou-taleb & Kawai, 2008; Fisher & Phillips, 2008; Gaysinsky & Weiss, 2007; Gutierrez, Barry-Ryan, & Bourke, 2008a; Lopez-Malo vigil et al., 2005; Nazef, Belguesmia, Tani, Prevost, & Drider, 2008; Patrignani et al., 2008; Periago, Conesa, Delgado, Fernndez, & Palop, 2006; Ponce, Roura, Del Valle, & Moreira, 2008; Raybaudi, Mosqueda-Melgar, & Martin-Belloso, 2008;Yamamoto, Matsunaga, & Friedman, 2004). Antimicrobials are used in food for two main reasons: (1) to control natural spoilage processes (food preservation), and (2) to prevent/control growth of micro-organisms, including pathogenic micro-organisms (food safety). Natural antimicrobials are derived from animal, plant and microbial sources. There is considerable potential for utilization of natural antimicrobials in food, especially in fresh fruits and vegetables. However, methods and mechanisms of action, as well as the toxicological and sensory effects of natural antimicrobials, are not completely understood (Burt, 2004; Davidson, 2006; Gaysinsky & Weiss, 2007; Gutierrez, Rodriguez, BarryRyan, & Bourke, 2008b; Lopez-Malo vigil et al., 2005; Moriera, Ponce, Del Valle, & Roura, 2007; Patrignani et al., 2008; Periago et al., 2006; Ponce et al., 2008; Raybaudi, Mosqueda-Melgar et al., 2008; Zaika, 1988). Even without a more comprehensive understanding of how natural antimicrobial substances work, there is a growing effort to develop new effective methods that rely primarily on their use to enhance food safety (Ayala-Zavala et al., 2008; Brandi et al., 2006; Chen et al., 2008; FAO/WHO Codex Alimentarius Commission., 2007; Liu, OConner, 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; Vagahasiya & Chanda, 2007).
In addition to their avoring effects, some spices and herbs have antimicrobial effects on plant and human pathogens (Brandi et al., 2006). Food processing technologies such as chemical preservatives cannot eliminate food pathogens such as Listeria monocytogenesis or delay microbial spoilage totally (Gutierrez, Barry-Ryan, & Bourke, 2009). Cold distribution of perishable food can help, but it cannot guarantee the overall safety and quality of the product. Moreover, changes in dietary habits and food processing practices and increasing demand for ready-to-eat products. Fruits and vegetables have been followed by increasing reports of food-borne pathogenic micro-organisms because of the presence of pathogens in raw materials (Lanciotti et al., 2004; Li, Tajkarimi, & Osburn, 2008; Li, Zhu et al., 2008). There are new techniques such as pulsed light, high pressure pulsed electric and magnetic elds for food preservation and controlling pathogens and spoilage micro-organisms in food. However, technologies such as mild heat processing, modiedatmosphere packaging, vacuum packaging and refrigeration are not sufciently effective, neither for eliminating undesirable pathogens nor delaying microbial spoilage. Moreover, some of these methods, such as vacuum cooling, can increase the probability of food contamination. Incorporation of natural antimicrobials into packaging materials, to protect the food surface rather than the food, has also been developed recently (Abou-taleb & Kawai, 2008; Fisher & Phillips, 2008; Gaysinsky & Weiss, 2007; Gutierrez et al., 2008a; Holley & Patel, 2005; Lanciotti et al., 2004; Li, Tajkarimi et al., 2008; Li, Zhu et al., 2008; Lopez-Malo vigil et al., 2005; Nazef et al., 2008; Patrignani et al., 2008; Periago et al., 2006; Ponce et al., 2008; Raybaudi, Mosqueda-Melgar et al., 2008; Raybaudi, Rojas-Grau, Mosqueda-Melgar, & Martin-Belloso, 2008). A growing body of data indicates that there is considerable potential for utilization of natural antimicrobials in food, especially application to fresh fruits and vegetables, for their oxidative degradation of lipids and improvement of the quality and nutritional value of food, in addition to their strong antifungal effects. EOs derived from spices and plants have antimicrobial activity against L. monocytogenes, Salmonella typhimurium, Escherichia coli O157:H7, Shigella dysenteriae, Bacillus cereus and Staphylococcus aureus at levels between 0.2 and 10 ll ml1(Burt, 2004). For example, combined mild heat treatment with addition of cinnamon and clove EOs to apple cider signicantly reduced the D-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, followed by treatment with high-intensity pulsed electric elds, successfully achieved the pasteurization level (reduction of at least 5.0 log10 units) (Mosqueda-Melgar, Raybaudi-Massilia, & Martin-Belloso, 2008a, 2008b). The purpose of this paper is to provide an overview of the data published mostly in the past 10 years on plant-derived compounds that have been reported to be effective against spoilage or pathogenic bacteria, and practical methods for screening these compounds.
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2. Historical overview of plant antimicrobials Natural antimicrobial agents derived from sources such as plant oils have been recognized and used for centuries in food preservation. EOs and spices were used by the early Egyptians and have been used for centuries in Asian countries such as China and India. Some of the spices, such as clove, cinnamon, mustard, garlic, ginger and mint are still applied as alternative health remedies in India. EO production can be traced back over 2000 years to the Far East, with the beginnings of more modern technologies occurring in Arabia in the 9th century. However, it was also during this time period that the medical applications of EOs became secondary to their use for avor and aroma. Plant extracts and spices, in addition to contributing to taste and avor, can act against Gram-positive pathogens such as L. monocytogenes. They can also enhance storage stability by means of active components including phenols, alcohols, aldehydes, ketones, ethers and hydrocarbons, especially in such spices as cinnamon, clove, garlic, mustard, and onion. The rst scientic studies of the preservation potential of spices, describing antimicrobial activity of cinnamon oil against spores of anthrax bacilli, were reported in the 1880s. Moreover, clove was used as a preservative to disguise spoilage in meat, syrups, sauces and sweetmeats. In the 1910s, cinnamon and mustard were shown to be effective in preserving applesauce. Since then other spices, such as allspice, bay leaf, caraway, coriander, cumin, oregano, rosemary, sage and thyme, have been reported to have signicant bacteriostatic properties (Burt, 2004; Ceylan & Fung, 2004; Gutierrez et al., 2008a; Jayaprakasha, Negi, Jena, & Jagan Mohan Rao, 2007; Kwon, Kwon, Kwon, & Lee, 2008; Soa, Prasad, Vijay, & Srivastava, 2007; Zaika, 1988). Most spices have eastern origins; however, some of them have been introduced after discovery of the New World spices such as chili peppers, sweet peppers, allspice, annatto, chocolate, epazote, sassafras, and vanilla, which have been used for food avoring and medicinal purposes (Ceylan & Fung, 2004).
of food products (Burt, 2004; Davidson, 2006; Gaysinsky & Weiss, 2007; Gutierrez et al., 2008a; Lopez-Malo vigil et al., 2005; Moriera et 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 antimicrobials are most commonly produced by SD (steam distillation) and HD (hydro distillation) methods, and alternative methods such as SFE (supercritical uid extraction) provide higher solubility and improved mass transfer rates. Moreover, the manipulation of parameters such as temperature and pressure leads to the extraction of different components when a particular component is required. Bioengineering of the EO components also provides more available commercial products (Burt, 2004). Edible, medicinal and herbal plants and spices such as oregano, rosemary, thyme, sage, basil, turmeric, ginger, garlic, nutmeg, clove, mace, savory, and fennel, have been successfully used alone or in combination with other preservation methods. They exert direct or indirect effects to extend foodstuff shelf life or as antimicrobial agent against a variety of Grampositive and Gram-negative bacteria However, their efcacy depends 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; Koutsoumanis, Lambropoulou, & Nychas, 1999; Sandasi, Leonard, & Viljoen, 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 possibly diterpenes with different groups of aliphatic hydrocarbons, acids, alcohols, aldehydes, acyclic esters or lactones (Fisher & Phillips, 2006). EOs and other plant extracts are principally responsible for antimicrobial activities in plants, herbs and spices. These extracts can be obtained from plants and spices by various methods, such as steam, cold, dry and vacuum distillation. These plant compounds, including glucosides, saponins, tannins, alkaloids, EOs, organic acids and others, are present as parts of the original plant defense system against microbial infection (Bajpai, Rahman, & Kang, 2008; Ceylan & Fung, 2004). Major components of the EOs can constitute up to 85%, and other components are usually at trace levels (Burt, 2004; Grosso et al., 2008). There are various chemical components present in plant-origin antimicrobials including, saponin and avonoids, thiosulnates, glucosinolates and saponins. Saponin and avonoids are found in fruits, vegetables, nuts, seeds, stems, owers, tea, wine, propolis and honey. They commonly form a soapy lather after shaking in water. The antimicrobial activity of saponins and avonoids in plants like oats (Avena sativa) and anthraquinones, carbohydrates and alkaloids derived from plants like Bersama engleriana (Melianthaceae) have been proven when extracted from roots, stem bark, leaves and wood (Bahraminejad, Asenstorfer, Riley, & Schultz, 2008; Cushnie & Lamb, 2005; Kuete et al., 2008; Musyimi, Muema, & Muema, 2008; Naidu, 2000a). Thiosulnates are prepared from garlic by mild procedures. They have strong antimicrobial activities against Gram-negative bacteria (Kim et al., 2008; Naidu, 2000a; Yoshida et al., 1999). Glucosinolates are present in broccoli, brussels sprouts, cabbage, and mustard powder and cause the pungent avor of mustard and horseradish. They demonstrate a wide range of antibacterial and antifungal properties with direct or synergistic effect in combination with other compounds (Almajano, Carbo, Lopez Jimenez, & Gordon, 2008; Graumann & Holley, 2008; Gutierrez et al., 2008a; Naidu, 2000a; Tolonen et al., 2004). Generally, phenolic compounds of EOs such as citrus oils extracted from lemon, olive oil (oleuropein) and tea-tree oil (terpenoids), orange and bergamot have broader antimicrobial effects and are not cate-
3. Major spice and herb antimicrobials Spices and EOs are used by the food industry as natural agents for extending the shelf life of foods. A variety of plant- and spice-based antimicrobials is used for reducing or eliminating pathogenic bacteria, and increasing the overall quality of food products. Plant-origin antimicrobials are obtained by various methods from aromatic and volatile oily liquids from owers, buds, seeds, leaves, twigs, bark, herbs, wood, fruits and roots of plants. EOs in plants generally are mixtures of several components. Some of those presence exert antimicrobial effects such as components in oregano, clove, cinnamon, citral, garlic, coriander, rosemary, parsley, lemongrass, sage and vanillin (Angioni et al., 2004; Arques et al., 2008; Daferera, Ziogas, & Polissiou, 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 ginger, black pepper, red pepper, chili powder, cumin and curry powder, showed lower antimicrobial properties (Holley & Patel, 2005). There are more than 1340 plants with dened antimicrobial compounds, and over 30,000 components have been isolated from phenol group-containing plant-oil compounds and used in the food industry. However, commercially useful characterizations of preservative properties are available for only a few EOs. There is a need for more evaluation of EOs in eld and food systems. Food-preservative utilization of spices and their EOs as natural agents has recently been focused on extending the shelf life of foods, reducing or eliminating pathogenic bacteria, and increasing overall quality
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gorized as spices. Meanwhile, there are increasing reports of nonphenolic compounds of oils, which are effective against both Gram-positive and Gram-negative groups, from oregano, clove, cinnamon, citral, garlic, coriander, rosemary, parsley, lemongrass, purple (cultivar Ison) and bronze (cultivar Carlos) muscadine seeds and sage (Angioni et al., 2004; Daferera et al., 2000; Davidson & Naidu, 2000; El-Seedi et al., 2008; Fisher & Phillips, 2006; Gutierrez et 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; Oussalah et al., 2004; Santos & Rao, 2001; Skocibusic et al., 2006; Yoshida et al., 1999). 4. Uses of plant-origin antimicrobials Food spoilage can occur from raw food materials to the processing and distribution. Spoilage sources might be chemical, physical and microbiological. Preservation techniques for microbiological spoilage have been dramatically improved in recent years to minimize any growth of micro-organisms including pathogenic micro-organisms (Gould, 1996). Research concerning plant-origin food-preservative EOs has increased since the 1990s, with more utilization of spices and their EOs as natural bio-preservatives, to increase shelf life and overall quality of food products and reduce or eliminate pathogenic micro-organisms (Burt, 2004; Moriera et al., 2007; Simitzis et al., 2008). Application of Thymus eigii showed stronger antimicrobial activity compared to vancomycin (30 mcg) and erythromycin (15 mcg) (Toroglu, 2007). Ginger (Zingiber ofcinale), galangal (Alpinia galanga), turmeric (Curcuma longa), and ngerroot (Boesenbergia pandurata) extracts against Gram-positive and Gram-negative pathogenic bacteria at 0.20.4% (v/v) for ngerroot and 810% (v/v) for all of the spices (Pattaratanawadee, Thongson, Mahakarnchanakul, & Wanchaitanawong, 2006). Cinnamon, cloves, and cumin showed the strongest antimicrobial effects against Staphylococcus aureus, Klebsiella pneumonia, Pseudomonas aeruginosa, Escherichia coli, Enterococcus faecalis, Mycobacterium smegmatis, Micrococcus luteus, and Candida albicans as test strains, with inhibition zones between <10 and >30 mm by the disc-diffusion method (Agaoglu, Dostbil, & Alemdar, 2007). a-Pinene, cineole, limonene, linalool and geranyl acetate are ve common antimicrobial compounds that have been effective against some food-borne pathogens and antibiotic-resistant Staphylococcus aureus, Bacillus cereus, Escherichia coli and Campylobacter jejuni (Chen et al., 2008; Sandasi et al., 2008). Spices such as allspice, bay leaf, caraway, coriander, cumin, cassia bark and liquorice have been reported to have signicant bacteriostatic/inhibition properties for patho-
genic and spoilage micro-organisms. Hydro-distilled EOs isolated from the oral parts of Nandina domestica Thunb showed potential activity against food-borne pathogenic and spoilage bacteria (Bajpai et al., 2008). Oregano, savory and thyme, which have terpenes, carvacrol, p-cymene, and thymol, have demonstrated antifungal and antimicrobial activity that has attracted attention recently because of their potential food safety applications, especially for oregano (Bendahou et al., 2008; Naidu, 2000b). Olive leaves (Olea europaea) showed antimicrobial effects against Campylobacter jejuni, Helicobacter pylori and Staphylococcus aureus (Sudjana et al., 2009). Ethanolic leaf extract of Lonicera japonica Thunb showed antimicrobial effects against some food-borne pathogens and potential use for food processing (Rahman & Kang, 2009). Thymus pallescent from different harvest locations showed different antimicrobial activities (Hazzit, Baaliouamer, Verissimo, Falerio, & Miguel, 2009). However, location has not shown a difference in antimicrobial/antioxidant activity of the Tunisian Thymus capitatus Hoff. et Link (Bounatirou et al., 2007). The antimicrobial activity of the eugenol oil (Eugenia caryophylata) containing phenolic compounds is considerably lower compared to similar chemical compounds (Amiri, Dugas, Pichot, & Bompeix, 2008). Allyl isothiocyanate is a non-phenolic volatile compound that showed similar effect at 9.4 ppm as mustard EOs in the culture medium with 12.3 ppm of the puried component (Turgis, Han, Caillet, & Lacroix, 2009). The presence of multiple phenolic phytochemicals from selected clonal herb species of the Lamiaceae family could prevent Staphylococcus aureus from developing antimicrobial resistance (Kwon, Apostolidis, Labbe, & Shetty, 2007). More than 400 spices have been used in the world, mostly in hotclimate countries (Ceylan & Fung, 2004). There are a variety of effective antimicrobial components in EOs derived from herbs such as oregano and thyme: carvacrol and p-cymene are two of them (Burt et al., 2007). Application of yarrow (Achillea. millefolium) as an ancient spice showed antimicrobial effect at 30% concentration against Staphylococcus aureus and Escherichia coli (Tajik & Jalali, 2009). Oregano and thyme, oregano with marjoram, and thyme with sage had the most effective EOs against Bacillus cereus, Pseudomonas aeruginosa, 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, which contain a high percentage of eugenol, carvacrol and/or thymol, are primarily responsible for bacteriocidal/bacteriostatic properties (Gutierrez, Rodriguez, Barry-Ryan, & Bourke, 2008b; Gutierrez et al., 2008a; Mandalari et al., 2007; Naidu, 2000b; Olonisakin, Oladimeji, & Lagide, 2007; Rodrguez et al., 2009). Table 1 presents some antimicrobial activities and components of spices and herbs.
Table 1 Spices, herbs and oils with antimicrobial activity and their avor components. Source: Adapted from Ceylan and Fung (2004), Holley et al. (2005), and Naidu (2000a). Category Herbs Species Basil, sweet (Ocimum basilicum) Oregano (Origanum vulgare) Rosemary (Rosmarinus ofnicalis) Sage (Salvia ofcinalis) Thyme (Thymus vulgares) Allspice, pimento (Pimenta diocia) Cinnamon (Cinnamonum zeylanicum) Clove (Syzgium aromaticum) Mustard (Brassica) Nutmeg (Myristica fragrans) Vanilla (Vanilla planifola, V. pompona, V. tahitensis) Olive oil Tea-tree oil (Melaleuca alternifolia) Plant part Leaves Leaves/owers Leaves Leaves Leaves Berry/leaves Bark Flower bud Seed Seed Fruit/seed Fruit Leaves Major avor component Linalool/methyl chavicol Carvacrol/thymol Camphor/1,8-cineole/borneol/camphor Thujone, 1,8-cinole/borneol/camphor Thymol/carvacol Eugenol/b-caryophyllene Cinnamic aldehyde/eugenol Eugenol Allyl isothiocyanate Myristicin/a-piene/Sabinene Vanillin (4-hydroxymethoxybenzaldehyde)/pOH-benzyl methyl ether) Oleuropein Terpenoids Bacterial inhibition (%) <50 75100 75100 5075 75100 75100 75100 75100 5075 5075
Spices
Oils
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4.1. Mechanism of action It has been demonstrated that the antimicrobial effects of the EOs acts by causing structural and functional damages to the bacterial cell membrane. It is also indicated that the optimum range of hydrophobicity is involved in the toxicity of the EOs (Goni et al., 2009). Spices and herbs are mostly used in the range of 0.050.1% (5001000 ppm) in food systems. Some spices have stronger antimicrobial activity than others and can be effective at 1000 ppm. However, some spices require higher concentrations (Ceylan & Fung, 2004). Application of antimicrobials by different exposure methods, such as vapor phase compared to direct contact method, of mustard and clove EOs showed noteworthy differences (Goni et al., 2009). The stereochemistry, lipophilicity and other factors affected the biological activity of these compounds which might be altered positively or negatively by slight modications (Veluri, Weir, Bais, Stermitz, & Vivanco, 2004). It has been shown that plant substances affect microbial cells by various antimicrobial mechanisms, including attacking the phospholipid bilayer of the cell membrane, disrupting enzyme systems, compromising the genetic material of bacteria, and forming fatty acid hydroperoxidase caused 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 isothiocyanate derived from mustard seems to have multi-targeted mechanisms of action in metabolic pathways, membrane integrity, cellular structure and statistically signicant higher release of the cell compounds of Escherichia coli O157:H7 (Turgis et al., 2009). Carvacrol increases the heat shock protein 60 HSP 60 (GroEL) protein and inhibited the synthesis of agellin highly signicantly in E. coli O157:H7 (Burt et al., 2007). There are concerns regarding the enhanced aroma and taste of oregano at the higher levels of application in food items, especially at 1% (Chouliara, Karatapanis, Savvaidis, & Kontominas, 2007). The inuence of seasonal harvest of plants, geographical location and altitude, storage and extraction procedures still has to be investigated in detail in order to be able to draw the utmost benet for nutritional and even more for industrial use (Proestos et al., 2008; Silva et al., 2007). Seasonal variations might have some effects on EOs of the cerrado species (Silva et al., 2007); however, they did not have a signicant effect on the EOs derived from Myrcia myrtifolia (De Cerqueira et al., 2007). The crude extract of Sorghum bicolor Moench has useful antimicrobial properties and plant extract and fractions showed variable antimicrobial properties (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 to in vitro trials: twofold differences in semi-skim milk, 10-fold in pork liver sausage, 50-fold in soup and 25100-fold in soft cheese. However, for Aeromonas hydrophila there was no difference between in vitro and in-food experiments on cooked pork and lettuce (Burt, 2004; Naidu, 2000a). The apparent antimicrobial efcacy of plantorigin antimicrobials depends on factors such as the method of extracting EOs from plant material, the volume of inoculum, growth phase, culture medium used, and intrinsic or extrinsic properties of the food such as pH, fat, protein, water content, antioxidants, preservatives, 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). Another important parameter regarding effects of food preservatives is ability to reduce the pH level inside the bacterial cell (pHin). It has been shown that pHin of both E. coli and Salmonella has been reduced by the effect of mustards EOs (Turgis et al., 2009). Generally, Gram-negative bacteria are less sensitive to the antimicrobials because of the lipopolysaccharide outer membrane of this 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 are usually more resistant to the plant-origin antimicrobials and even show no effect, compared to Gram-positive bacteria (Rameshkumar, 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 sum of the individual effects, this is synergy; antagonism happens when a combination shows less effect compared to the individual applications (Burt, 2004). Synergistic effects of some compounds, in addition to the major components in the EOs, have been shown in some studies (Abdalla, Darwish, Ayad, & El-Hamahmy, 2007; Becerril, Gomez-Lus, Goni, Lopez, & Nerin, 2007; Rota, Herrera, Martinez, Sotomayor, & Jordan, 2008). Application of a certain combination of carvacrol-thymol can improve the efcacy of EOs against pathogenic micro-organisms (Lambert, Skandamis, Coote, & Nychas, 2001). Synergism between carvacrol and p-cymene, a very weak antimicrobial, might facilitate carvacrols transportation into the cell by better swelling the B. cereus cell wall (Burt, 2004). Antimicrobial activity of combination of cinnamon and clove EOs in vapor phase showed better antimicrobial with less active concentration in the vapor phase compare to liquid phase (Goni et al., 2009). Thymol and carvacrol showed synergistic and antagonistic effects, in different combinations of cilantro, coriander, dill and eucalyptus EOs (each containing several components) and mixtures of cinnamaldehyde and eugenol, against Staphylococcus sp., Micrococcus sp., Bacillus sp. and Enterobacter sp. (Burt, 2004). An antagonistic effect on Bacillus cereus was seen in rice when carvacrol and p-cymene were used with salt; high-hydrostatic pressure showed a synergistic effect in combination with thymol and carvacrol against L. monocytogenes (Burt, 2004). Vacuum packing in combination with oregano EOs showed a synergistic effect against L. monocytogenes with 23 log10 reduction. Similar results have been recorded when clove and coriander EOs have been used against Aeromonas hydrophila on vacuumpacked pork. Application of oregano EO has a synergistic effect in modied-atmosphere packaging (MAP) including 40% CO2, 30% N2 and 30% O2 (Burt, 2004). The available oxygen is another factor antagonistic on EO activities; by decreasing the oxygen level, the sensitivity of micro-organisms to the EOs has been increased (Burt, 2004). Residual hydrosols after distillation of EOs from plant materials can be used as economical sources of antimicrobial components (Lis-Balchin et al., 2003). Table 3 summarizes the results of various experiments regarding application of plant-origin antimicrobials in food. Table 4 demonstrates some aspects and studies in the area of plant-derived antimicrobials; due to methodological differences, such as choice of plant extract(s), test micro-organism(s) and antimicrobial test method, these ndings are not directly comparable. Application of nisin with carvacrol or thymol has been positively effective against Bacillus cereus with temperatures increasing from 8 C to 30 C (Burt, 2004). Application of nisin with rosemary extract enhanced the bacteriostatic and bactericidal activity of the nisin (Thomas & Isak, 2006). Oregano EOs, in combination with modied-atmosphere packaging, have effectively increased the shelf life of fresh chicken (Chouliara et al., 2007). Antimicrobial resistance did not develop in Yersinia enterocolitica and Salmonella choleraesuis after sub-inhibitory passes with cinnamon, by direct contact or vapor phase (Goni et al., 2009). Combination of linalool and 1, 8cineole (1:1) created more resistance in E. coli, compared to application of pure linalool. Either synergism or antagonism of 1, 8-cineole and linalool derived from Cinnamosma fragrans could happen against Gram-negative bacteria and Fusarium oxysporu (Randrianarivelo et al., 2009). The synergistic effect of different components could offer a way to prevent possible off avor caused by clove and tea tree when used to protect against Escherichia coli O157:H7 and minimize
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Table 2 Some reported sources of natural antimicrobials in plant within the last 10 years. Plant name Coriander (Coriandum sativum), Oregano (Origanum vulgare), Rosemary (Rosmarinus ofcinalis), Parsley (Petroselinum crispum) Effective against Gram-positive and Gram-negative bacteria, including Listeria monocytogenes Reference 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), and Santos and Rao (2001) 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) 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) Ceylan and Fung (2004) and Skocibusic et al. (2006)
Allipse (Pimenta dioica), Basil (Ocimum basilicum), Blue mallee (Eucalyptus polybractea), Bay (Laurus nobilis), Caraway seed (Carum carvil), Lemongrass (Cymbopogon citratus), Lemon balm(Melissa ofcinalis), Marijoram (Origanum majorana), Rosemary(Rosmarinus ofcinalis), and Sage (Salvia ofcinalis) Clove (Syzygium aromaticum) Sage (Salvia ofcinalis), Cinnamon (Cinnamomum zeylanicum) and Marijoram (Origanum majorana), Allipse (Pimenta dioica)
Bacillus subtilis, Clostridium botulinum, Escherichia coli, Listeria monocytogenes, Salmonella typhimurium and Staphylococcus aureus
Pathogens such as Bacillus subtilis, Clostridium botulinum, Escherichia coli, Listeria monocytogenes, Salmonella typhimurium, Staphylococcus aureus Broad spectrum antibacterial effect against Gram-positive and Gram-negative pathogenic micro-organisms Staphylococcus spp.
Basil (Ocimum basilicum), Bay (Laurus nobilis), and Lemongrass (Cymbopogon citratus) Blackberry (Rubus spp.), Bay (Laurus nobilis), Basil (Ocium basilicum), Cilantro (immature leaves of Coriandrum sativum), Coriander (Coriandrum sativum seeds), Cinnamon (Cinnamomum zeylanicum), Coriander (Coriandum sativum), Marijoram (Origanum majorana) and Thyme (Thymus vulgaris) Oregano (Origanum vulgare), Sage (Salvia ofcinalis), Thyme (Thymus vulgaris) and Satureja hortensis L. Marjoram (Origanum majorana) Cumin (Cuminum cyminum)
Burt (2004), Greule and Mosandl (2008), Gutierrez et al. (2008a, 2008b), Lopez-Malo vigil et al. (2005), and Romeo et al. (2008)
Staphylococcus aureus and Escherichia coli Alternative for synthetic preservatives routinely used in the food industry Bacillus cereus, Bacillus subtilis, Clostridium botulinum, Listena monocytogenes, Pseudomonas uorescens, Salmonella enteritidis, Staphylococcus aureus Clostridium botulinum, Pseudomonas aeruginosa, Staphylococcus aureus, Yersinia enterocolitica Bacillus cereus, Clostridium botulinum, Salmonella enteritidis, Staphylococcus aureus, Yersinia enterocolitica Broad spectrum antibacterial effect against Gram-positive and Gram-negative pathogenic micro-organisms Broad spectrum antibacterial effect against Gram-positive and Gram-negative pathogenic micro-organisms Escherichia coli, Salmonella typhimurium, Shigella dysenteriae, Staphylococcus aureus
Bousmaha-Marroki et al. (2007), Burt (2004), and Razzaghi-Abyaneh et al. (2008) Mahmoud et al. (2007) Ceylan and Fung (2004)
Dill (Anethum graveolens)
Ceylan and Fung (2004)
Fennel (Foeniculum vulgare)
Garlic (Allium vineale)
Mint (Mentha piperita)
Onion (Allium cepa)
off avor effects in meat products (Moriera et al., 2007). Combinations of EOs of oregano and thyme, oregano with marjoram and thyme with sage had the most effects against Bacillus cereus, Pseudomonas aeruginosa, Escherichia coli O157:H7 and L. monocytogenes (Gutierrez et al., 2008a). 5. Review of some ndings of in vitro experiments In vitro experiments on plant-origin antimicrobials are well described in the literature. However, the antimicrobial activity of herbs and spices might vary based on the tested organism (Bagamboula, Uyttendaele, & Debevere, 2003). Below are some examples of reported ndings organized by the target microbial species. 5.1. A. hydrophila This is the most sensitive to antimicrobials among Gram-negative 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 uid extract of the shiitake mushroom Lentinula edodes (Kitzberger, Smania, Pedrosa, & Ferreira, 2007), hydro-distilled fresh leaves of Pittosporum neelgherrense Wight et Arn (John, George, Pradeep, & Sethuraman, 2008), leaves, bark and fruits of Neolitsea scheri (John et al., 2008), EOs of the ower heads and leaves of Santolina rosmarinifolia L. (Compositae) (Ionnouy et al., 2007), different extracts of thyme, hydro distillation of Syzygium gardneri leaves (Raj et al., 2008), aerial parts of fresh Plectranthus cylindraceus oil (Mohsenzadeh, 2007), EOs of Actinidia macrosperma (Lu, Zhao,
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Table 3 Inhibitory activities of plant-origin antimicrobials against pathogenic bacteria, protein toxins and fungi, listed alphabetically representative studies conducted within the last 10 years. Organism Bacillus cereus Adverse effects Food poisoning; emesis Inhibitors Tea, eugenol, leaf volatile oil, bark volatile oil; bark oleoresin, E-cinnamaldehyde, clove, mustard, cinnamon, Melianthaceae (Bersama engleriana), oil-macerated garlic, Petiveria alliacea L. root extract, Aristolochia indica L., tannins, dried and commercial garlic products, garlic oil, marjoram and basil essential oils, citral, linalool and bergamot vapor, methanol and acetone extracts of 14 plants belonging to different families References 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), Winward et al. (2008), Yoshida et al. (1999), and Yilmaz (2006)
Bacillus subtilis
Food poisoning
Teas, leaf volatile oil, leaf oleoresin, eugenol, bark Kong, Wang, and Xiong (2007), Li, Zhu et al. (2008), volatile oil; bark oleoresin, E-cinnamaldehyde, oilSingh et al. (2007), Vagahasiya and Chanda (2007), macerated garlic extract, tannins, polymers of avanols, Yoshida et al. (1999), and Yilmaz (2006) cassia bark-derived substances, crude extracts of bulbs (Lycoris chinensis), stems and leaves of (Nandina domestica), (Mahonia fortunei), (Mahonia bealei), stems of Berberis thunbergii and stems, leaves and fruits of Camptotheca acuminata, methanol and acetone extracts of 14 plants belonging to different families Black and green tea, cinnamaldehyde and carvacrol Friedman (2007), Arques et al. (2008), and Ravishankar, Zhu, Law, Joens, and Friedman (2008) 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 and Holley (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-Grau et al. (2007), Singh et al. (2007), Seydim and Sarikus (2006), Sivakami and Rupasinghe (2007), Tolonen et al. (2004), Vagahasiya and Chanda (2007), and Winward et al. (2008)
Campylobacter jejuni
Food poisoning; diarrhea Food poisoning; diarrhea
Escherichia coli
Cinnamon, oregano oil (Oreganum vulgare), pure essential oils, leaf volatile oil, eugenol, bark volatile oil, bark oleoresin, E-cinnamaldehyde, carvacrol, oregano oil, citra, lemongrass oil, cinnamaldehyde, cinnamon oil, [Oregano in whey protein isolate (WPI) lms containing, at 2% level, garlic essential oil at 3&4%], lemongrass, thyme, carvacrol, cinnamaldehyde, citral, and thymol, clove (Eugenia caryophyllata), glucosinolates naturally present in mustard powder, mustard, Bersama engleriana (Melianthaceae), chrysanthemum extracts, cabbage juice, Petiveria alliacea L. roots, Aristolochia indica L., catechin, chlorogenic acid and phloridzin, ground yellow mustard, Brassica oleracea juice, dried garlic powder, commercial garlic products, and garlic oil, onion, marjoram and basil essential oils, Scutellaria, Forsythia suspensa (Thunb), and rosemary and clove oil with 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) and Camptotheca acuminata (stems, leaves and fruits), methanol and acetone extracts of 14 plants belonging to different families, caffeine, 1,3,7-trimethylxanthine. Tea, pure essential oils, [Oregano in whey protein isolate (WPI) lms containing at 2% level, garlic essential oil at 3&4%], cabbage juice, cinnamon bark, cinnamon leaf, and clove, Brassica oleracea juice, lemon balm and sage essential oils, cassia bark-derived substances, citral, linalool and bergamot vapor Catechins, Bersama engleriana (Melianthaceae)
Listeria monocytogenes
Food poisoning; listeriosis
Brandi et al. (2006), Cava et al. (2004), Fisher and Phillips (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 Pseudomonas aeruginosa
Tuberculosis
Friedman (2007), Kuete et al. (2008)
Food spoilage Tea extract, [Milk protein-based edible lms containing Friedman (2007), Hammer et al. (1999), Lambert et al. oregano, 1.0% (w/v), pimento, or 1.0% oregano pimento (2001), Li et al. (2008), Oussalah et al. (2004), and Yilmaz (2006) (1:1)], tannins, polymers of avanols, lemongrass, oregano and bay, crude extracts of Lycoris chinensis (bulbs), Nandina domestica/Mahoniafortunei/Mahonia bealei (stems and leaves), Berberis thunbergii (stems) and Camptotheca acuminata (stems, leaves and fruits), certain combinations of carvacrol-thymol, oregano essential oil; methanol and acetone extracts of 14 plants belonging to different families Food spoilage Teas, [Milk protein-based edible lms containing oregano, 1.0% (w/v) pimento, or 1.0% oregano pimento(1:1)], tannins, polymers of avanols Diarrhea Friedman (2007), Oussalah et al. (2004), and Yilmaz (2008)
Pseudomonas uorescens
Shigella spp. Tea
Tea, Bersam engleriana(Melianthaceae), tannins, Arques et al. (2008), Friedman (2007), Kuete et al. polymers of avanols, crude extracts of Lycoris chinensis (2008), Li, Zhu et al. (2008), and Yilmaz (2006) (bulbs), Nandina domestica/Mahonia fortunei/Mahonia bealei (stems and leaves), Berberis thunbergii (stems) and Camptotheca acuminata (stems, leaves and fruits) (continued on next page)
1206 Table 3 (continued) Organism Adverse effects
Inhibitors
References
Salmonella spp.
Food Teas, leaf volatile oil; leaf oleoresin; eugenol; bark poisoning; volatile oil; bark oleoresin, E-cinnamaldehyde, [oregano Salmonellosis in whey protein isolate (WPI) lms containing at 2% level, garlic essential oil at 3&4%], oregano (Origanum vulgare), and cinnamon (Cinnamomum zeylanicum), lemongrass, thyme (Thymus vulgaris), carvacrol, cinnamaldehyde, citral, and thymol), methanol extract of Aspilia mussambicensis (Compositae), Bersama engleriana (Melianthaceae), Aristolochia indica L., Brassica oleracea juice, dried garlic powder, commercial garlic products, and garlic oil, marjoram and basil essential oils, cassia bark-derived substances, lemongrass, bay, methanol and acetone extracts of 14 plants belonging to different families, thymol Food poisoning Food poisoning; infection Catechins Theasinensin, tea, cinnamon, oregano (Origanum vulgare), pure essential oils, leaf volatile oil, leaf oleoresin, eugenol, bark volatile oil, bark oleoresin, Ecinnamaldehyde, [oregano in whey protein isolate (WPI) lms containing at 2% level, garlic essential oil at 3% and 4%], dried garlic powder, commercial garlic products, clove, mustard, rosemary (Rosmarinus ofcinalis), lemon balm (Melissa ofcinalis), sage (Salvia ofcinalis), chocolate mint (Mentha piperata), and oregano (Origanum vulgare), Bersama engleriana (Melianthaceae), chrysanthemum extracts, oil-macerated garlic extract, Petiveria alliacea L. root extract, Aristolochia indica L., tannins, polymers of avanols, lemongrass and bay; certain combinations of carvacrol- thymol, citral, linalool and vapor, methanol and acetone extracts of 14 plants belonging to different families Tea extract Basil, clove, garlic, horseradish, marjoram, oregano, rosemary, thyme, cassia bark-derived substances Teas, pure essential oils
Davidson and Naidu (2000), Friedman (2007), Gutierrez et al. (2008a), 2008b), Hammer et al. (1999), Kong et al. (2007), Kuete et al. (2008), Singh et al. (2007), Seydim and Sarikus (2006), Vagahasiya and Chanda (2007), and Yoshida et al. (1999)
Spore forming bacteria Staphylococcus aureus
Friedman (2007) Arques et al. (2008), Ben Sassi et al. (2008), Fisher and Phillips (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), Musyimi et al. (2008), Singh et al. (2007), Seydim and Sarikus (2006), Vagahasiya and Chanda (2007), Winward et al. (2006), Yilmaz (2006), and Yoshida et al. (1999)
V. cholerae V. parahaemolyticus Yersinia enterocolitica Toxins Botulinum Cholera Molds Aspergillus avus
Cholera Mild gastroenteritis Diarrhea
Arques et al. (2008) Kong et al. (2007) and Yano et al. (2006) Friedman (2007), Lopez et al. (2007)
Neurotoxin botulism Cholera
Black tea Catechins, theaavins
Friedman (2007) Friedman (2007)
Mycotoxicosis Ochratoxins Mycotoxicosis
Pure essential oils, leaf oleoresin, leaf volatile oil, eugenol, bark volatile oil, bark oleoresin, Ecinnamaldehyde, cassia bark-derived substances Methanol extract of Aspilia mussambicensis (Compositae) Thymol
Kong et al. (2007) and Lopez et al. (2007)
Aspergillus niger Aspergillus parasiticus
Musyimi et al. (2008) Davidson and Naidu (2000)
Wang, Chen, & Fu, 2007), specic derivative from the fruits of Eucalyptus globulus (Tan et al., 2008), EOs from thymol and carvacrol at1:2000 dilutions and cinnamic aldehyde and eugenol extracted from cinnamon and clove at 0.11.0% w/v, 0.06% v/v concentration(Davidson & Naidu, 2000), aerial parts of Ammoides atlantica (Coss. et Dur.) Wolf. (Apiaceae) (Laouer et al., 2008), leaves, bark and fruits of Neolitsea scheri (John et al., 2008), hydro-distilled dried and oil samples of Thymus caramanicus (Nejad Ebrahimi et al., 2008), and EOs from Anzer teas and wild-grown leaves of Acorus calamus (Radusiene, Judzentiene, Peciulyte, & Janulis, 2007; Sekeroglu, Deveci, Buruk, Gurbuz, & Ipek, 2007). Extracts of different spices, evaluated by disc diffusion assay, had the following relative inhibitory effects on Bacillus cereus: clove > mustard > cinnamon > garlic > ginger > mint (Soa et al., 2007).
5.3. C. jejuni It has been shown that Campylobacter jejuni is more sensitive to natural antimicrobials compared to other pathogenic microorganisms (Sudjana et al., 2009). Linalool vapor of bergamot and linalool oils (Fisher & Phillips, 2008), cinnamic aldehyde and eugenol extracted from cinnamon and clove at 0.05% concentration, linalool and methyl chavicol vanillin extracted from sweet basil vanilla at 0.25% concentration (Davidson & Naidu, 2000). EO of Origanum minutiorum with a capacity as a food preservative showed a variety of antimicrobial effects against Campylobacter jejuni (Aslim & Yucel, 2007). The ciprooxacin resistance of Campylobacter strains has been shown to be strongly diminished by application of EO of Origanum minutiorum (Aslim & Yucel, 2007).
M.M. Tajkarimi et al. / Food Control 21 (2010) 11991218 Table 4 Some studies regarding application of EOs or their components in-food studies conducted in the past 10 years. Food group Meat and poultry Meat EO or component Clove oil , eugenol and coriander, oregano, thyme oils, encapsulated rosemary EO, clove and tea tree Oregano and thyme, oregano with marjoram and thyme with sage Chinese cinnamon and winter savory EOs EOs and nisin Oregano, pimento, or oregano:pimento Marjoram (Origanum majorana L.) EO Eugenol Sage oil Oregano Bacterial species Listeria monocytogenes, Aeromonas hydrophila, Escherichia coli O157:H7 B. cereus and P. aeruginosa, Escherichia coli O157:H7 and Listeria monocytogenes Pathogenic micro-organisms Listeria monocytogenes Escherichia coli O157:H7 or Pseudomonas spp. Several species of bacteria Listeria monocytogenes, Aeromonas hydrophila, Bacillus cereus, Staphylococcus aureus, Salmonella typhimurium Increase shelf life Inhibitory effect Yes (+++) Reference Burt (2004) and Moriera et al. (2007) Du and Li (2008)
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Fried meat
Yes (+)
Ground beef Meat Meat surfaces Fresh sausage Chicken Chicken Chicken
Yes (increased radiosensitivity) Yes Yes Yes Yes (+++++) No Yes (with modiedatmosphere packaging) No No No No Yes (encapsulated has more effect than standard) Yes (in combination with other techniques)
Turgis et al. (2008) Solomakos et al. (2008) Mosqueda-Melgar et al. (2008a, 2008b), and Oussalah et al. (2004) Burt (2004) Burt (2004) Burt (2004) Chouliara et al. (2007)
Pate Minced pork Vacuum-packed ham Vacuum-packed minced pork Liver pork sausage
Mint oil Thyme oil Cilantro oil Oregano oil Rosemary
Listeria monocytogenes, Salmonella enteritidis Listeria monocytogenes Listeria monocytogenes Clostridium botulinum spores Listeria monocytogenes
Burt (2004) Burt (2004) Burt (2004) Burt (2004) Hayouni, Chraief et al. (2008)
Minced pork
Winter savory (Satureja montana) EO
Food-borne bacteria and improve quality
Carraminana et al. (2008)
Fish Cooked shrimp Red grouper llet, cubed Cod llets Salmon llets Cods roe salad Coated semi-fried tuna slices Fresh-water sh Lightly salted cultured sea bream (Sparus aurata) llets Carp llets Carp Carp
Thyme oil, cinnamaldehyde Carvacrol, citral, geraniol Oregano oil Oregano oil Mint oil Eugenol and linalool Wild-thyme hydrosol Oregano
Pseudomonas putida Salmonella typhimurium Photobacterium phosphoreum Photobacterium phosphoreum Salmonella enteritidis Increased shelf life Increased shelf life, preservative effect Increased shelf life, antioxidant activity
Very slight Yes (+++) Yes (+) No Yes (+++) Yes Yes Yes
Burt (2004) Burt (2004) Burt (2004) Burt (2004) Burt (2004) Naidu (2000a) Oral et al. (2008) Goulas and Kontominas (2007)
Carvacrol + Thymol Thymol, carvcarol and cinnamaldehyde Allyl isothiocyanate, carvacrol, cinnamaldehyde, citral, cuminnaldehyde, eugenol, isoeugenol, linalool and thymol
Four times increased shelf life Increased shelf life Increased shelf life
Yes Yes (+++) Yes (+)
Mahmoud, Kawai, Yamazaki, Miyashita, and Suzuki (2006) Mahmoud et al. (2004) Mahmoud et al. (2004)
Dairy Mozzarella cheese Semi-skimmed milk Soft cheese
Clove oil Carvacrol DMC Base Natural preservative comprising 50% EOs of rosemary, sage and citrus
Listeria monocytogenes Listeria monocytogenes Listeria monocytogenes
Yes (+) Yes (+) From 1.0 ll g1(+)
Burt (2004) Burt (2004) Burt (2004)
(continued on next page)
1208 Table 4 (continued) Food group Yoghurt EO or component
Bacterial species Streptococcus thermophilus
Inhibitory effect Yes (Mint oil +, Cardamom, clove: ++, Cinamon:+++) From 1.5%v/w ++ Yes Yes
Reference Burt (2004)
Clove, cinnamon, cardamom, peppermint oil Mint oil Satureja cilicica essential oil Oregano, thyme, rosemary, sage, cumin and clove
Tzatziki (yogurt and cucumber salad) Butter Dairy industries
Salmonella enteritidis Antioxidant Starter cultures and related food spoilage
Burt (2004) Ozkan et al. (2007) Viuda-Martos et al. (2008)
Vegetables Lettuce, romaine Carrots Lettuce, iceberg green Eggplant salad Alfalfa seeds
Thyme oil Thyme oil Basil methyl chaviol (BMC) Oregano oil Cinnamaldehyde, thymol
E. coli O157:H7 E. coli O157:H7 Natural ora E. coli O157:H7 Salmonella spp., six serotypes
Yes (+) Yes (+++) Yes (++) Yes (++) Yes (50 C: +, 70 C: 0)
Burt (2004) Burt (2004) Burt (2004) Burt (2004) Burt (2004)
Rice Boiled rice Boiled rice Rice
Carvacrol Sage oil Ocimum basilicum
Natural ora Bacillus cereus, Staphylococcus aureus, Salmonella typhimurium Three stored-rice pests (Sitophilus oryzae, Rhyzopertha dominica and Cryptolestes pusillus)
Yes (+++) No Yes
Burt (2004) Burt (2004) Lopez et al. (2008)
Fruit Kiwifruit Honeydew melon
Carvacrol, cinnamic acid Carvacrol, cinnamic acid
Natural ora Natural ora
Yes (+++) Yes (0+)
Burt (2004) Burt (2004)
5.4. Clostridium perfringens Clove EOs have an inhibitory effect against Clostridium perfringens at 0.4% (v/w) concentration (Davidson & Naidu, 2000). 5.5. Escherichia coli A variety of antimicrobial effects on Escherichia coli has been shown by: guarana extract (Majhenic et al., 2007), chloroform extract of the plant of Abrus precatorious L. roots at 84% concentration (Zore et al., 2007), EOs from leaves, stems and owers of Salvia reuterana (Lamiaceae) (Esmaeili et al., 2008), linalool vapor of bergamot and linalool oils (Fisher & Phillips, 2008),water-distilled EO from leaves and owers of Micromeria nubigena H.B.K. (Lamiaceae) (El-Seedi et al., 2008), hydro distillation leaf oil of Cinnamomum chemungianum (Raj et al., 2008), Rosmarinus ofcinalis oil (Gachkar et al., 2007), anzer tea EOs (Sekeroglu et al., 2007), EOs of Actinidia macrosperma (Lu et al., 2007), oleuropein extracted from olive oil at 0.4 mg/ml concentration; clove EOs at 0.4% (v/w) concentration; thymol and carvacrol EOs at 5%, 10%, 15%, 20% concentration, and cinnamic aldehyde and eugenol extracted from cinnamon and clove at 0.05% and 0.04% concentrations (Davidson & Naidu, 2000), linalool and methyl chavicol vanillin extracted from sweet basil vanilla at 0.25% concentration; terpenes extracted from teatree oil at 0.120.25% v/v concentration (Davidson & Naidu, 2000), aerial parts of Ammoides atlantica (Coss. et Dur.) Wolf. (Apiaceae) (Laouer et al., 2008), mango seed kernel (Abdalla et al., 2007), EOs of the ower heads and leaves of Santolina rosmarinifolia L. (Compositae) (Ionnouy et al., 2007), sorghum extracts and fractions (Kil et al., 2009), and hydro-distilled fresh leaves of Pittosporum neelgherrense Wight et Arn (John et al., 2008). Extracts and oil extracts of various spices had relative inhibitory effects on Escherichia coli as follows: mustard > clove > cinnamon > garlic > ginger > mint (Soa et al., 2007).
5.6. L. monocytogenes Rosmarinus ofcinalis oil showed a strong antimicrobial effect against L. monocytogenes (Gachkar et al., 2007). Thymol and carvacrol EOs showed inhibitory effects against L. monocytogenes at 24 C in a microbiological medium at 0.50.7 w/v and were bacteriostatic at 0.51.0% concentration; and borneol extracted from sage and rosemary had inhibitory effect against L. monocytogenes at 0.020.05% concentration (Davidson & Naidu, 2000). 5.7. Molds and yeasts Some EOs demonstrate a broad range of natural fungicidal effects against post-harvest pathogens, especially because of their bioactivity in the vapor phase for storage applications (Tripathi, Dubey, & Shukla, 2008). However, more time is needed for vapor-phase bioactivity effect, possible absorption into the food material needed to be considered (Fisher & Phillips, 2008). Antifungal activity might be affected by the targeted fungal physiological activity (Daferera et al., 2000). The reported effective compounds against food-borne fungi, including Aspergillus niger; A. avus; and A. parasiticus are: guarana extract (Majhenic et al., 2007), EO and methanol extract of Satureja hortensis (Dikbas, Kotan, Dadasoglu, & Sahin, 2008), Satureja hortensis L. containing carvacrol and thymol (Razzaghi-Abyaneh et al., 2008), water-distilled EO from leaves and owers of Micromeria nubigena H.B.K. (Lamiaceae) (El-Seedi et al., 2008), oleuropein extracted from olive oil at 0.2 mg/ml concentration, EOs from thymol at 500 lg/ml concentration and at 1.0% and 100 lg/ml concentrations; cinnamic aldehyde and eugenol extracted from cinnamon and clove at 1.0% and 100 lg/ml concentrations (Davidson & Naidu, 2000), Aspergillus parasiticus growth and Aatoxins production has been inhibited by Thymus vulgari and Citrus aurantifolia, whereas Mentha spicata L., Foeniculum miller, Azadirachta indica A.
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Juss, Conium maculatum and Artemisia dracunculus has only inhibited the fungal growth, while Carum carvi L. has controlled aatoxin production without effect on the fungal growth (RazzaghiAbyaneh et al., 2009), linalool and methyl chavicol vanillin extracted from sweet basil vanilla at 2000 lg/ml concentration (Davidson & Naidu, 2000) . Hydro-distilled EOs of stems, leaves (at vegetative and owering stages) and owers of Eugenia chlorophylla O. Berg. (Myrtaceae) (Stefanello et al., 2008), various extracts of thyme (Davidson & Naidu, 2000; Nejad Ebrahimi et al., 2008), were active against molds and yeasts. Oleoresin extracted from cinnamon and cinnamic aldehyde and eugenol extracted from cinnamon and clove inhibited mycotoxin-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 and clove showed antifungal effects. Smaller phenolic compounds, such as allyl isothiocyanate and citralon in mustard and lemongrass, have been more effective as volatiles (Suhr & Nielsen, 2003); however, in EOs such as marjoram oil, they have been effectively antifungal in a matrix with mainly hydrocarbons (Daferera et al., 2000). 5.8. Pseudomonas sp. Pseudomonas, specically Pseodumonas aeruginosa are the least sensitive group of bacteria to the action of EOs and bioactive components of plant-origin (Burt, 2004; Ceylan & Fung, 2004). Bioactive components of plant-origin antimicrobials are relatively weak against Pseudomonas spp. (Ceylan & Fung, 2004). However, susceptibility of all except Pseudomonas aeruginosa to the Origanum genus has been shown (Bendahou et al., 2008). Hydro-distilled EOs from leaves, stems and owers of Salvia reuterana (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 scheri (John et al., 2008), oils of air-dried samples obtained by hydro distillation of Thymus caramanicus (Nejad Ebrahimi et al., 2008) were active against Pseudomonas spp. Antibacterial activity of the oil isolated by hydro distillation of Syzygium gardneri leaves was effective against Gram-negative bacterial species such as Pseudomonas uorescens (Raj et al., 2008). Guarana extract (Majhenic et al., 2007) and leaves, bark and fruits of Neolitsea scheri (John et al., 2008) were active against Pseudomonas uorescens. 5.9. Salmonella sp. and Shigella sp. The below components has been reported as effective compounds against Salmonella sp. or Shigella sp: the oil isolated by hydro distillation of Syzygium gardneri leaves and leaf oil of Cinnamomum chemungianum (Raj et al., 2008), hydro-distilled EOs of fresh leaves and mature fruits of Pittosporum viridulum (John, Karunakaran, George, Pradeep, & Sethuraman, 2007), EOs of Iranian avoring, Zataria multiora Boiss(Akhondzadeh Basti, Misaghi, & Khaschabi, 2007), syringic acid, isorhamnetin and quercetin, three compounds extracted from dried fruit of Ardisia elliptica Thunb (Phadungkit & Luanratana, 2006), oleuropein extract, cinnamic aldehyde and eugenol extracted from cinnamon and clove at 0.05% and 0.04% concentration, linalool and methyl chavicol vanillin extracted from sweet basil vanilla at 0.1% concentration , Terpenes extracted from tea-tree oil at 0.120.25% v/v concentration (Davidson & Naidu, 2000), leaves bark and fruits of Neolitsea scheri (John et al., 2008, hydro-distilled EOs of fresh leaves and mature fruits of Pittosporum viridulum (John et al., 2007).
According to a study on MuellerHinton (MH) Agar and MH broth, cloves showed antimicrobial effect against Shigella sonnei, Shigella exneri and E. coli at 1% weight/volume concentration (Bagamboula et al., 2003). 5.10. Staphylococcus aureus A variety of antimicrobial activities against Staphylococcus aureus: Chloroform and ethanol fractions of Abrus precatorious L. roots was 93% (percentage of inhibition) effective (Zore et al., 2007), hydro-distilled EOs from leaves, stems and owers of Salvia reuterana (Lamiaceae) (Esmaeili et al., 2008), EOs from an alpine needle leaf of Abies koreana (Jeong, Lim, & Jeon, 2007), hydro-distilled extract of Syzygium gardneri leaves (Raj et al., 2008), hydro-distilled EOs of fresh leaves and mature fruits of Pittosporum viridulum (John et al., 2007), EOs from an alpine needle leaf of Abies koreana (Jeong et al., 2007), Rosmarinus ofcinalis oil (Gachkar et al., 2007); EOs of Zataria multiora Boiss (Akhondzadeh Basti et al., 2007), EOs of Actinidia macrosperma (Lu et al., 2007), oleuropein extracted from olive at 0.1% w/v concentration of the extract delayed growth of the bacteria at 0.40.6% w/v concentration; clove EOs at 0.4% (v/ w) concentration; EOs from thymol and carvacrol 5%, 10%, 15%, and 20% concentration, EOs from thymol and carvacrol at 175 225 lg/ml concentration; cinnamic aldehyde and eugenol extracted from cinnamon and clove at 0.03% and 0.04% concentrations, linalool and methyl chavicol vanillin extracted from sweet basil vanilla at 0.1% concentration, terpenes extracted from teatree oil at 0.120.25% v/v concentration (Davidson & Naidu, 2000), aerial parts of Ammoides atlantica (Coss. et Dur.) Wolf. (Apiaceae) (Laouer et al., 2008), leaves, bark and fruits of Neolitsea scheri (John et al., 2008), water-distilled EOs from leaves and owers of Micromeria nubigena H.B.K. (Lamiaceae) (El-Seedi et al., 2008), Curcuma domestica and Curcuma viridiora at ratios of 20/15 (Chen et al., 2008), anzer teas EOs (Sekeroglu et al., 2007), EOs of the ower heads and leaves of Santolina rosmarinifolia L. (Compositae) (Ionnouy et al., 2007), and hydro-distilled EOs of fresh leaves and mature fruits of Pittosporum viridulum (John et al., 2007). 5.11. Vibrio parahaemolyticus EOs from thymol and carvacrol at 0.5% concentration as whole spices and 100 lg/ml as essential oil (Davidson & Naidu, 2000), tannins and polymers of avanols (Yilmaz, 2006), and Curcuma domestica and Curcuma viridiora at ratios of 18/15 (Chen et al., 2008) showed antimicrobial activity against Vibrio parahaemolyticus. 5.12. General Gram-positive and Gram-negative bacteria Mint (Mentha piperita) EO was more effective against S. enteritidis compared to L. monocytogenes when in Greek appetizers taramosalata and tzatziki. In another study, using freshly distilled EOs showed more susceptibility to Gram-positive bacteria compared to Gram-negative (Burt, 2004). Lemon, orange and bergamot EOs and their components (Fisher & Phillips, 2006), Hydro-distilled EOs of stems, leaves (at vegetative and owering stages) and owers of Eugenia chlorophylla O. Berg. (Myrtaceae) are effective against Gram-positive bacteria (Stefanello et al., 2008). Phlomis species from the Lamiaceae family, borneol extracted from sage and rosemary had an inhibitory effect against Gram-positive and Gram-negative bacteria at 2% concentration for two groups, 0.3% bacteriostatic and 0.5% bactericidal for Gram-positive bacteria (Bajpai et al., 2008). Linalool and methyl chavicol vanillin extracted from sweet basil vanilla showed inhibitory effect against 3335 bacteria, yeasts and molds (Davidson & Naidu, 2000).
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Bergamot peel (Mandalari et al., 2007) is effective against gramnegative bacteria. Origanum oil, extracted by steam distillation from Thymus capitatus L. (Labiatae) by Hoffmanns and Link (common name: Spanish oregano; synonyms: Coridothymus capitatus or Thymus capitatis), at 486 mg/L concentration in treated-grey-water reed-bed efuent, can prevent coliform re-growth for up to 14 days (Winward, Avery, Stephenson, & Jefferson, 2008). Antimicrobial activity 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 carvacrol chemotypes) was active against 10 pathogenic micro-organisms (Sabulal, George, Pradeep, & Dan, 2008). Generally, Gram-positive bacteria are more sensitive to saponin, with MIC (minimum inhibitory concentration) between 0.3 and 1.25 mg/ml, compared to 1.255 mg/ml for Gram-negatives (Oleszek, 2000). MIC of oregano EOs were lower than thyme and cinnamon EOs, against Gram-negative pathogenic micro-organisms (Escherichia coli, Yersinia enterocolitica, Pseudomonas aeruginosa, and Salmonella choleraesuis) compared to Gram-positive ones (Listeria monocytogenes, Staphylococcus aureus, Bacillus cereus, and Enterococcus faecalis) as well as molds (Penicillium islandicum and Aspergillus avus) (Lopes-Lutz et al., 2008; Lopez, Sanchez, Battle, & Nerian, 2007). 6. Some in-food experiments with plant-origin antimicrobials In-food studies depend on several additional factors, which have not been tested in similar in vitro studies (Stoicov, Saffari, & Houghton, 2009). Spices and herbs can be used as an alternative preservative and pathogen-control method in food materials. Application of both extracts and EOs of plant-origin antimicrobials such as oral parts of Nandina domestica Thunb could be a potential alternative to synthetic preservatives (Bajpai et al., 2008). Generally, effective EOs in decreasing order of antimicrobial activities are: oregano > clove > coriander > cinnamon > thyme > mint > rosemary > mustard > cilantro/sage (Burt, 2004). However, in another study, mint showed less antimicrobial effect compared to mustard (Soa et al., 2007). There are differences between in vitro and in-food trials of plant-origin antimicrobials, mainly because only small percentages of EOs are tolerable in food materials. Finding the most inhibitory spices and herbs depends on a number of factors such as type, effects on organoleptic properties, composition and concentration and biological properties of the antimicrobial and the target micro-organism and processing and storage conditions of the targeted food product (Gutierrez et al., 2008a; Naidu, 2000a; Romeo, De Luca, Piscopo, & Poiana, 2008). In a study on blanched spinach and minced cooked beef, using clove and teatree EOs, three and four times the MIC in in vitro studies were needed to restrict E. coli O157:H7 populations in the food materials (Moriera et al., 2007). Despite some positive reports in regard to application of plant-origin natural antimicrobials, two major issues are faced regarding application of plant-origin antimicrobials in food: odors created mostly by the high concentrations, and the costs 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 of pathogens associated with meat products. However, some authors have recorded low antimicrobial effects against pathogens in contaminated meat products (Grosso et al., 2008). High-fat-content of the food materials has effects on the application of EOs (Burt, 2004; Lis-Balchin et al., 2003). It may be because of the lipid solubility of EOs compared to aqueous parts of food (Lis-Balchin et al., 2003). Combination of 1% cloves and oregano in broth culture showed inhibitory effect against L. monocytogenes, however, the
same concentration was not effective in meat slurry (Lis-Balchin et al., 2003). According to Table 4, recent studies regarding certain oils such as eugenol and coriander, clove, oregano and thyme oils showed high effect against L. monocytogenes, Aeromonas hydrophila and autochthonous spoilage ora in meat products. However, mustard, cilantro, mint and sage oils were less effective or ineffective (Burt, 2004). A 520 ll g1 level of eugenol and coriander, clove, oregano and thyme oil inhibits growth of L. monocytogenes, Aeromonas hydrophila and autochthonous spoilage ora in meat products (Burt, 2004). Survival and growth of both susceptible and antibiotic-resistant Campylobacter strains have been inhibited effectively on agar plates 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 compared to standard rosemary EOs against L. monocytogenes in pork liver sausage; neither the direct effect of the level used nor manner and effect of encapsulation are reported (Carraminana, Rota, Burillo, & Herrera, 2008). The activity of oregano EOs against Clostridium botulinum spores in combination with low levels of sodium nitrite enhanced the delay of growth of bacteria more than the sodium nitrite alone, depending on the number of inoculated spores (Burt, 2004). EOs extracted from the aerial parts of cultivated Salvia ofcinalis L. were effective against Salmonella enteritidis (Hayouni et al., 2008). Winter savory (Satureja montana) EOs in combination with other preservation methods such as reduced temperature, pulsed light, high pressure, pulsed electric and magnetic elds, irradiation, or packaging under a modied atmosphere can be utilized as economical natural antibacterial substance to control growth of foodborne bacteria and improve quality of minced pork (Carraminana et al., 2008). Chinese cinnamon and winter savory EOs were used successfully to increase radio sensitivity in ground beef (Turgis, Borsa, Millette, Salimieri, & Lacroix, 2008). Combinations of EOs and nisin showed enhanced antimicrobial activities against L. monocytogenes (Solomakos, Govaris, Koidis, & Botsoglou, 2008). Rancidity of heat-treated turkey-meat products was inhibited by aqueous extract of rosemary, sage and thyme (Mielnik, Sem, Egelandsdal, & Skrede, 2008). Treatments (homogenization) of meat with oregano and sage EO signicantly reduced oxidation, while the heat treatment and storage time signicantly affected the antioxidant activity of the meat (Fasseas, Mountzouris, Tarantilis, Polissiou, & Zervas, 2007). Milk protein-based edible lms containing oregano, pimento, or oregano/pimento were effective against Escherichia coli O157:H7 or Pseudomonas sp. on meat surfaces (Mosqueda-Melgar et al., 2008a; Mosqueda-Melgar et al., 2008b; Oussalah et al., 2004). Chlorophyll-containing lms were tested against Staphylococcus aureus and Listeria monocytogenes, showing that it was possible to reduce growth of these micro-organisms inoculated in cooked frankfurters by covering the frankfurters with sodium magnesium chlorophyllin-gelatin lms and coatings (Lpez-Carballo, Hernndez-Muoz, Gavara, & Ocio, 2008). Marjoram (Origanum majorana L.) EOs were effective against several species of bacteria in fresh sausage (Busatta et al., 2008). Chlorophyllins are semi-synthetic porphyrins obtained from chlorophyll. Chlorophyllin-gelatin lms and coating applications successfully reduced Staphylococcus aureus and L. monocytogenes in cooked frankfurter (Lpez-Carballo et al., 2008). Individual extracts of clove, rosemary, cassia bark and liquorice demonstrated strong antimicrobial activity; but the mixture of rosemary and liquorice extracts was the best inhibitor against all four types of microbes (L. monocytogenes, Escherichia coli, Pseudomonas uorescens and Lactobacillus sake) in modied atmosphere-packaged fresh pork and vacuum-packaged ham slices stored at 4 C (Zhang, Kong, Xiong, & Sun, 2009). Santalum album, Cinnamomum cassia, and Artemisia capillaris were the most effective antimicrobials
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in raw sheep meat (Luo et al., 2007). There are potential bio-preservative capabilities for application of clove and tea-tree oils to control Escherichia coli O157:H7 on blanched spinach and minced cooked beef (Moriera et al., 2007). 6.2. Fish The high fat content of some sh, as with meat products, reduces the antibacterial effect of EOs against various micro-organisms; however, some of the EOs had positive effects even in the high-fat-content shes. For example, oregano oil is more effective against the spoilage organism Photobacterium phosphoreum on cod llets than on salmon, which is a fatty sh. Oregano oil is more effective than mint oil in/on sh, even in fatty-sh dishes. Application of EOs on the surface of whole sh or as coating for shrimps inhibited Salmonella Enteritidis, L. monocytogenes and natural spoilage ora (Burt, 2004; Hayouni & Chraief et al., 2008). There is signicant preservative and increased shelf-life effects of wild thyme (Thymus serpyllum), about 15 to 20 days with freshwater sh (Oral, Gulmez, Vatansever, & Guven, 2008). Strong antioxidant activity of oregano has been shown in a study by Goulas and Kontominas (2007). Shelf life of carp llets was extended fourfold by application of combined carvacrol + thymol with some other additives, compare to sterile 0.2% agar solution as a control (Mahmoud, Kawai, Yamazaki, Miyashita, & Suzuki, 2007). Antimicrobial activity studies of garlic oil and nine compounds of EOs against bacterial isolates from carp showed that thymol, carvacrol and cinnamaldehyde had the strongest antimicrobial activities, followed by isoeugenol, eugenol, garlic oil, and then citral for increasing the shelf life of carp llets, respectively (Mahmoud et al., 2004). Essential oils of Aloysia sellowii were successfully screened against a variety of Gram-positive and -negative micro-organisms and two yeasts in brine shrimp (Simionatto et al., 2005). The freshness indicator of tuna slices showed even better results after coating with an edible solution containing 0.5% eugenol plus 0.5% linalool, compared to controls (Abou-taleb & Kawai, 2008). Basil, clove, garlic, horseradish, marjoram, oregano, rosemary, and thyme have been used successfully to implement hurdle technology for protecting seafood from the risk of Vibrio parahaemolyticus contamination (Yano et al., 2006). A synergistic effect of treatment with anodic electrolyzed NaCl solution, combined with eugenol and linalool, has been found to enhance shelf-life extension of coated semi-fried tuna (Abou-taleb & Kawai, 2008). 6.3. Dairy products It has been shown that extract of mango seed kernel could reduce total bacterial count, inhibit coliform growth, exert remarkable antimicrobial activity against an Escherichia coli strain and extend the shelf life of pasteurized cow milk (Abdalla et al., 2007). High water activity positively affects the application of EOs in milk by speeding the transfer and movement of EOs toward the targeted micro-organisms (Cava, Nowak, Taboada, & Marin-Iniesta, 2007). The antimicrobial activity of terpenes is not or is only marginally involved in the explanation of the inuence of the botanical composition of meadows on the sensory properties of pressed cheeses (Tornambe et al., 2008). Satureja cilicica essential oil can serve in butter as both a natural antioxidant and aroma agent (Ozkan, Simsek, & Kuleasan, 2007). EOs from oregano, thyme, rosemary, sage, cumin and clove were tested on the growth of six bacteria, four of them used as starters and two of them as spoilage-causing bacteria (Viuda-Martos et al., 2008). Cinnamon, cardamom and clove oils inhibit the growth of yoghurt starter cultures more than mint oil; however, in other study mint oil was effective against Salmonella enteritidis in low-fat yoghurt and cucumber salad (Burt, 2004). An in vitro study on twelve ethanol extracts of propolis showed antimicrobial and
antifungal activity especially at low levels against pathogenic micro-organisms to protect starter culture strains in fermented products (Kalogeropoulos, Konteles, Troullidou, Mourtzinos, & Karathanos, 2009). EOs of Melaleuca armillaris are effective against lactic acid bacteria and may serve to improve the quality of food products, depending on the LAB strain, as well as on the concentration of the EOs (Hayouni, Bouix, Abedrabba, Leveau, & Hamdi, 2008). EOs of clove, cinnamon, bay and thyme were tested against L. monocytogenes and Salmonella enteritidis in soft cheese; clove oil was found more effective against Salmonella enteritidis in full-fat cheese than in cheese slurry (Burt, 2004). 6.4. Vegetables Application of antimicrobial activity of EOs in vegetables has shown more successful results against natural spoilage ora and food-borne pathogens in washing water, due to the low fat content of the products. It can be enhanced by decreasing the pH of the food and/or temperature. For example, oregano oil was effective against Escherichia coli O157:H7 and reduced nal populations in eggplant salad (Burt, 2004). Cinnamaldehyde and thymol were effective against six Salmonella serotypes on alfalfa seeds. Increasing temperature reduced the effectiveness of these antimicrobials, perhaps because of volatility decreasing permeability of the antibacterial compounds in the liquid media (Burt, 2004; Cava et al., 2007; Goni et al., 2009). 6.5. Rice Leaves of ve different varieties of Ocimum basilicum were effective against three stored-rice pests (Sitophilus oryzae, Rhyzopertha dominica and Cryptolestes pusillus) (Lopez, Jordan, & Pascual-Villalobos, 2008). Sage oil and carvacrol were successfully used against Bacillus cereus in rice (Burt, 2004). Ocimum gratissimum and Thymus vulgaris have been used successfully against two major seed-borne fungi of rice in Cameroun (Nguefack et al., 2007). 6.6. Fruit Natural ora on kiwi fruit (pH 3.23.6) was effectively inhibited by carvacrol and cinnamaldehyde but less effectively on honeydew melon (pH 5.45.5), which may result from the difference of pH between the fruits (Burt, 2004). Natural fungicidal plant volatiles have been found more effective, compared to similar synthetic preservatives, against post-harvest fungal disease caused by Botrytis cinerea in stored grapes (Tripathi et al., 2008). EOs incorporated into an alginate-based edible coating of fresh-cut Fuji apples showed more than 4-log reduction in the population of E. coli O157:H7. A total inhibition of native microora for 30 days at 5 C, for preservation, taste, quality and pathogen control of the product has been shown. The most 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, and lemongrass EOs and their active compounds cinnamaldehyde, eugenol, and citral have also shown promising antimicrobial and quality effects on fresh-cut melon (Raybaudi, Mosqueda-Melgar et al., 2008). Application of a combination of cinnamon and eugenol was tested for control of the germination of alicyclobacillus spores. The application of 40 ppm cinnamaldehyde with 40 ppm of eugenol or 80 ppm eugenol by itself preserved apple juice for 7 days (Bevilacqua, Corbo, & Sinigglia, 2010). Polyphenols are present in green, white and commercial tea and are key antimicrobial and antioxidant components for fresh-cut apple (Abou-taleb & Kawai, 2008). Combination of cinnamaldehyde and eugenol as an apple juice preservative against Alicyclobacillus acidoterrestris showed more acceptable results in the test panels (Bevilacqua et al., 2010).
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6.7. Animal feed Application of thymol in animal feed shows effects on the bacterial community in animal feed (Janczyk, Trevisi, Souffrant, & Bosi, 2008). EO compounds showed limited effects on nutrient utilization in studies of alfalfa silage and corn silage as the sole forage source in ruminants (Benchaar et al., 2007). Effects of cinnamon leaf oil on total volatile fatty acid (VFA) concentration have been studied. It was concluded that it inhibits propionate-producing bacteria and might have an adverse effect on metabolism and productivity of ruminants (Fisher & Phillips, 2008).
7. Effectiveness determinations Comparison of published data regarding different methods is complicated: according to some investigators there is increased variation based on extraction method, culture medium, size of inoculum, choice of emulsier and basic test method (Soa et al., 2007). Antimicrobial activity in most experiments has been quantied on two bases, MIC and MBC (minimum bactericidal concentration), which is presumably greater than the MIC. MIC is dened in different terms; some of them are lowest concentration resulting in maintenance or reduction of inoculums viability, lowest concentration
Table 5 Different screening methods for evaluating activity of plant-origin antimicrobials against different food-borne pathogenic micro-organisms studies conducted within the last 10 years. Food-borne pathogen Bacillus cereus, Pseudomonas aeruginosa and Escherichia coli Method Inhibitors Reference Arques et al. (2008)
Adjusted suspensions of micro-organisms were placed in Catechins proper agar and solidify the mixture in Petri plates, sterile discs were inserted into the plates. And proper volume solution of each extract were transferred to the discs and incubated at proper temperature and time Direct contact assay method in order to dene Minimum Inhibitory Concentration (MIC). Cinnamon or oregano
Escherichia coli and Staphylococcus aureus Escherichia coli and Staphylococcus aureus Bacillus cereus Bacillus cereus, Escherichia coli O157:H7, Listeria monocytogenes and Salmonella enterica
Becerril et al. (2007) Ben Sassi et al. (2008) Friedman (2007)
Modied disc-diffusion method originated from Jorgensen, Four strains of Tunisian Turnidge, and Washington (1995) Chrysanthemum species LuriaBertani (LB) agar plates The modied bactericidal assay described previously by Friedman, Henika, Levin, Mandrell, Kozukue (2006) Tea avonoids
Extract of oregano leaves with added Friedman, garlic juice and oregano oil Henika, Levin, & Mandrell (2007) Different ethanol extracts of soices honeysuckle, Scutellaria, Forsythia suspensa (Thunb), cinnamon, rosemary and clove oil Kong et al. (2007)
Escherichia coli and Pseudomonas uorescens
Well-diffusion test described by Kim, Marshall et al. (1995)
Gram-negative, Gram-positive bacteria and molds Modied vapor diffusion test which is explained in detail by Isidorov and Vinogorova (2005) Escherichia coli, Bacillus cereus and Pseudomonas uorescens Bacillus cereus, Pseudomonas aeruginosa and Escherichia coli Campylobacter jejuni
Three commercially available Lopez et al. essential oils (EOs) cinnamon ,thyme, (2007) and oregano Majhenic et al. (2007) Musyimi et al. (2008) Ravishankar et al. (2008)
Method described by Janssen, Scheffer, and Baerheim Guarana seed extract Svendsen (1987) and Vagi, Simandi, Suhajda, and Hethelyi (2005) Pit and disc methods according to Rajakanuna, Harris, and Methanol extract of Aspilia Towers (2002) mossambicensis (Compositae) Different concentrations of main constituents of plantderived cinnamon and oregano oils, in sterile phosphatebuffered saline Modied method explained by Friedman, Henika, and Mandrell (2002), Friedman, Henika, Levin, and Mandrell (2004) Growth zone-inhibition developed method described by Davidson and Parish (1989) Zone of inhibition assay on solid medium Cinnamaldehyde and carvacrol
Escherichia coli
Oregano oil/carvacrol; cinnamon oil/ Rojas-Grau cinnamaldehyde; and lemongrass oil/ et al. (2007) citral Volatile oils and oleoresin of Cinnamomum zeylanicum Blume (leaf and bark) Oregano, rosemary and garlic essential oils Singh et al. (2007) Seydim and Sarikus (2006)
Bacillus cereus, Bacillus subtilis Staphylococcus aureus, Escherichia coli, Salmonella typhi and Pseudomonas aeruginosa Salmonella enteritidis, Escherichia coli O157:H7, Listeria monocytogenes and Staphylococcus aureus
Escherichia coli, Staphylococcus aureus and Bacillus Disc-diffusion technique cereus Escherichia coli Salmonella typhimurium, Pseudomonas aeruginosa, Escherichia coli, Staphylococcus aureus, Bacillus cereus, Bacillus subtilis and Salmonella typhimurium Vibrio parahaemolyticus and Escherichia coli Agar plate method Agar disc-diffusion method (Nair, Kalariya, & Chanda, 2005)
Six Indian spice extracts: clove, Winward et al. cinnamon, mustard, garlic, ginger and (2008) mint Cabbage juices Tolonen et al. (2004)
Methanol and acetone extracts of 14 Vagahasiya plants belonging to different families and Chanda (2007) 18 Plant species Yano et al. (2006)
Screening growth or survival of these two bacteria at different temperatures in nutrient-rich medium and dened pH
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required for complete inhibition of test organism up to 48 h incubation, lowest concentration inhibiting visible growth of test organism, or lowest concentration resulting in a signicant decrease in inoculums viability (>90%). MBC is dened as concentration where 99.9% or more of the initial inoculum is killed or lowest concentration at which no growth is observed after sub-culturing into fresh broth. The MIC method is cited by most researchers, but some quote MBC as a measure of antibacterial performance (Brandi et al., 2006; Romeo et al., 2008). MICs for carvacrol, thymol, eugenol, perillaldehyde, cinnamaldehyde and cinnamic acid were in the range of 0.055 ll m1 in vitro (Burt, 2004). The in vitro EO studies using agar to determine MICs are generally are the same order of magnitude. The optical density (OD) (turbidity) measurement and the enumeration of colonies by viable count are the most-used methods. The redox indicator resazurin has been used recently in a new microdilution method (Burt, 2004). New approaches and advances in extraction methods, such as crude extraction, high-intensity ultrasound-assisted (HI-US) in combination with proper solvent selection, can improve these approaches (Burt, 2004; Ibrahim, Tse, Yang, & Fraser, 2009; Romeo et al., 2008; Thongson, Davidson, Mahakarnchanakul, & Weiss, 2004). Thirty-eight strains of Salmonella have been tested with some modications in the diffusion technique to evaluate antimicrobial activity of chive extract (Ibrahim et al., 2009). The most-used methods for quantitative and qualitative evaluation of EOs of plants and spices are in vitro or exploratory (endpoint and descriptive methods) and applied (inhibition curves and endpoint methods). Diffusion, dilution or bio-autographic methods are categories of antimicrobial activity tests (Brandi et al., 2006). However, there are some observed anomalies in screening of antimicrobial activity against Staphylococcus aureus, with a greater reduction of growth at the MIC than at the MBC (Becerril et al., 2007). Moreover, there are differences among publications between deni-
tions and among procedures used in preparation of the tested samples (Brandi et al., 2006; Burt et al., 2007; Kim et al., 2006). Methods such as solvent-free microwave extraction (SFME) and application of crude extracts and enzyme conversions of herbs and spices will improve efcacy and extraction rates, with shorter extraction times and higher levels of active antimicrobial components. Crude extracts of herbs and plants have demonstrated oxidative degradation and antioxidant properties (Bendahou et al., 2008; Ibrahim et al., 2009; Kahkonen et al., 1999; Mandalari et al., 2007). In SFME method, a microwave is used and a plant material is inserted into an extraction vessel with hexane, more detailed information is provided in Bendahou et al. (2008). Vapor-phase experiments are more reliable methods in determining antimicrobial properties; in this method the concentration is expressed as weight per unit volume (mg/l air), and the sterile blank lter disc is placed in the center of the lid of the Petri dish (Goni et al., 2009). The disc-agar-diffusion method, drop-agar diffusion method and direct-contact technique in agar are the usual techniques in the screening approach, which has been described in detail in other references (Burt, 2004). Identication of antimicrobial activity is signicantly affected by the method of assay and may be interfered with by various food components and/or addition of compounds such as bovine serum albumin (BSA) (Burt, 2004; Davidson & Naidu, 2000). High-pressure extraction (with pure CO2 and with co-solvent) was more effective method than low pressure to obtain extracts (Kitzberger et al., 2007). Other techniques in antimicrobial determination are: dilution of the EO in agar or broth which showed similar approaches between methods and denitions, broth-dilution studies with bacterial enumeration by optical density (OD) (turbidity) measurement, and application of the redox indicator resazurin as a visual indicator of the MIC (Brandi et al., 2006; Holley & Patel, 2005). Table 5
Table 6 Antibacterial activity of various concentrations of spices, as a function of the screening method.a Spice Concentration (%)b Bacillus cereus Discc Cinnamon 0.5 1 2 3 0.5 1 2 3 0.5 1 2 3 0.5 1 2 3 0.5 1 2 3 0.5 1 2 3 10.3 0.5 11.0 0.0 11.3 0.5 12.0 0.0 10.3 0.5 11.3 0.5 12.6 0.5 16.0 0.0 11.6 0.5 12.6 0.5 14.0 0.0 14.3 0.5 9.6 0.5 10.3 0.5 11.0 0.0 11.6 0.5 11.3 0.5 14.6 1.1 14.6e 0.5 18.3e 1.1 10.3 0.5 11.6 0.5 15.6 0.5 Well/cupd 10 0 11.6 0.5 13.3 0.5 14.6 0.5 23.6 0.5 25.6 0.5 10.6 0.5 10.3 0.5 11.3 0.0 13.3 0.5 14.0 0.0 14.6e 0.5 16.6e 0.5 9.6 0.5 10.3 0.5 11.3 0.5 Escherichia coli Disc 8.0 0.0 10.0 0.0 12.3 0.5 14.3 0.5 11.6 0.5 13.3 0.5 15.6 0.5 19.3 0.5 10.0 1.0 10.0 0.0 11.3 0.5 12.3 0.5 9.3 0.5 10.3 0.5 10.6 0.5 11.3e 0.5 13.3 0.5 15.0e 1.0 16.3e 0.5 11.6 0.5 19.3 0.5 21.6 0.5 25.6 0.5 Well/cup 10.6 0.5 12.6 0.5 14 1 16.3 0.5 17.3 0.5 20.3 0.5 23.3 0.5 10.3 0.5 12.3 0.5 13.0 1.0 13.0 0.0 10.0 0.0 11.3 0.5 8.6e 0.5 9.3e 0.5 80 12.6 0.5 14.6 0.5 19.3 0.5 Staphylococcus aureus Disc 10.0 0.0 11.6 0.5 12.6 0.5 16.3 0.5 10.6 0.5 12.0 0.0 12.3 0.5 14.0 1.0 10.6 1.1 11.3 0.5 13.0 1.0 14.6 0.5 12.6 0.5 14.3 0.5 15.0e 1.0 17.3e 0.5 10.3 0.5 11.6 0.5 14.3 0.5 16.0 1.0 Well/cup 10 0 10.6 0.5 12.3 0.5 18.3 0.5 23.6 0.5 25.6 0.5 10.3 0.5 11.6 0.5 10.6 0.5 12.3 0.5 13.3 0.5 14.6 0.5 26.6e 0.5 27.6e 0.5 8.3 0.5 9.6 0.5
Clove
Garlic
Ginger
Mint
Mustard
Differences between different concentrations within a spice found to be signicant at P < 0.05. Adapted 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.
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demonstrates some different screening methods for evaluating the antimicrobial activity of different plant-origin antimicrobials against different food-borne pathogenic micro-organisms. 7.1. Disc-diffusion method The Food and Drug Administration (FDA) has been approved this method as a standard for the National Committee for Clinical Laboratory Standards (Turker & Usta, 2008). The disc-diffusion method is the most often-used technical method for antimicrobial screenings of EOs. Antimicrobial activity is generally evaluated by this method for preliminary studies. In this method, a paper disc soaked with the EO is placed on the inoculated surface of an agar plate and the zone of microbial inhibition is measured. Different parameters in this test could affect the result, such as the volume of EO on the paper discs, the thickness of the agar layer and the solvent. For example, some of reported solvents are ethanol, methanol, Tween-20, Tween-80, acetone in combination with Tween-80, polyethylene glycol, propylene glycol, n-hexane and dimethyl sulfoxide, which could result in difculties when comparing different studies (Brandi et al., 2006; Burt et al., 2007). More precise data regarding extract antimicrobial evaluation have been obtained with this method (Kil et al., 2009). Table 6 shows antimicrobial activities against Escherichia coli, Bacillus cereus, and Staphylococcus aureus measured by the 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, & Veness, 1997). The inhibition zones of EOs against food-borne and other pathogens have been measured by this method (Saif Mokbel & Suganuma, 2006). This was the method used for testing antimicrobial activity of extracts from aerial parts of seven wild sages from Western Canada Artemisia absinthium L., Artemisia biennis Willd, Artemisia cana Pursh, Artemisia dracunculus L., Artemisia frigida Wlld, Artemisia longifolia Nutt. and Artemisia ludoviciana Nutt. against bacteria, yeasts and fungi, including Escherichia coli, Staphylococcus aureus, Candida albicans and Aspergillus niger (Lopes-Lutz et al., 2008). 7.3. Broth microdilution method The broth microdilution method was used for antimicrobial activity evaluation of aerial parts of fresh Plectranthus cylindraceus oil against Staphylococcus aureus and Bacillus subtilis (Mohsenzadeh, 2007). According to Davidson and Naidu (2000), this method showed lower MICs (% v/v) of different essential oils extracted from bay, clove, peppermint and thyme against Escherichia coli, Staphylococcus aureus and Candida albicans, compared to agar-dilution assay. This method was used by Radusiene et al. (2007) to evaluate the antimicrobial activity of Acorus calamus against 17 species of bacteria, yeasts and fungi. 7.4. Direct-contact technique in agar The direct-contact technique in agar has been used for screening the antimicrobial activity of carvacrol, the EO produced from Thymus ciliatus sp. eu-ciliatus, against Staphylococcus aureus and Escherichia coli (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 avoring
and preservation purposes. Spices and herbs, which were originally added for improving taste, can also naturally and safely improve shelf life of food products (Holley & Patel, 2005). There are a variety of methods for testing the antimicrobial activities of spices, herbs and their components. These methods strongly affect the observed level of inhibition; there is a difference in activity against micro-organisms between each individual and or combination of spices and herbs. Various reasons may contribute in the differences between results, including inconsistency between analyzed plant materials even in the same leaves (Radusiene et al., 2007). The low pH level might work as a result of direct effect of the pH or the effect on EOs on the lipid phase of the bacterial membrane (Abou-taleb, & Kawai, 2008; Akhondzadeh Basti et al., 2007). Organoleptic and safety issues in application of the EOs in food must be addressed. Application of traditional and natural antimicrobials has been recently outlined by regulatory agencies in the US. Based on Code of Federal Regulation 21 CFR part 182.20, EOs of cinnamon, clove, lemon grass and their respective active compounds (cinnamaldehyde, eugenol and citral, respectively) are generally recognized as safe (GRAS) (Raybaudi, RojasGrau et al., 2008; Turgis et al., 2009). Application of Vapor phase combination of Eos showed successful results for an antimicrobial packaging development with less active components of cinnamon and clove (Goni et al., 2009). Changes in avor due to application of antimicrobial components are a major issue. However, avor has not been affected after application of eugenol oil (Eugenia caryophylata) against four apple pathogens in fresh-cut apple (Amiri et al., 2008). Application of edible and bio-base lms with different EOs in the packaging process of sausage casing and processed cheese slices will need further investigation (Seydim & Sarikus, 2006). However, some materials, such as thymol, have not been recognized as food-grade additives by European legislation (Falcone, Speranza, Del Nonile, Corbo, & Sinigaglia, 2005). In the EU countries, EOs as avorings have been registered and recognized as safe-to-use materials: carvacrol, carvone, cinnamaldehyde, citral, p-cymene, eugenol, limonene, menthol and thymol are in this group; however, two EO components, estragole and methyl eugenol, have been deleted from the safe list in 2001. Application of whole EOs seems to be more feasible for most countries, due to the costs of procedures to evaluate safety of any added avoring materials (Burt, 2004). Synergism and antagonism of these materials need to be further investigated before their broad application in the food industry. It is necessary to dene a target and effective range for each EO, including MIC and safety data (toxicity, allergenicity) in food materials (Svoboda et al., 2006). Application of plant-origin antimicrobials needs to be addressed by regulatory authorities for most parts of these compounds. Assessment of the effect of high doses of some EOs on intestinal cells, as well as cost and odors created by high concentrations of these materials, also should be considered seriously. Several successful combined methods of application of these EOs in conjunction with new approaches such as hurdle technology and modied-atmosphere packaging created pleasant odor with longer shelf life (Burt, 2004; Davidson, 2006; Fisher & Phillips, 2008; Friedman, 2007; Goulas & Kontominas, 2007; Naidu, 2000a; Proestos et al., 2008; Silva et al., 2007). According to Lanciotti et al. (2004), other possible ways to reduce the organoleptic impact include: (1) Minimizing perception of the presence of spices/herbs and EOs 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 cell membrane.
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Evaluation of new preservatives such as natural antimicrobials in food, evaluating food structure, composition and interaction between natural microora and food-borne disease agents could be made much more precise by application of predictive models (Koutsoumanis et al., 1999). Several studies have been focused on the application of individual EOs derived from plants. Some studies showed whole EOs have more antimicrobial activity compared to the mixture of major components (Burt, 2004). However, information on the effects of these natural compounds in combination and or as crude extracts against food-borne micro-organisms is limited (Ibrahim et al., 2009; Mandalari et al., 2007). The future will see much-needed investigation of food applications of the naturally occurring antimicrobials, especially the effectiveness of EOs, individually and in combination with other parts of plant extract, other effective EOs and other food-processing techniques.
References
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Food Control 21 (2010) 11991218

Contents lists available at ScienceDirect

Antimicrobial herb and spice compounds in food

Keywords: Herbs and spices Natural preservatives Food-borne pathogens

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

1212 1214 1214 1214 1214 1214 1215

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

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

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

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

Dill (Anethum graveolens)

Ceylan and Fung (2004)

Fennel (Foeniculum vulgare)

Ceylan and Fung (2004)

Garlic (Allium vineale)

Ceylan and Fung (2004)

Mint (Mentha piperita)

Ceylan and Fung (2004)

Onion (Allium cepa)

Ceylan and Fung (2004)

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

Food poisoning; diarrhea Food poisoning; diarrhea

Food poisoning; listeriosis

Mycobacterium tuberculosis Pseudomonas aeruginosa

Friedman (2007), Kuete et al. (2008)

Shigella spp. Tea

1206 Table 3 (continued) Organism Adverse effects

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

Spore forming bacteria Staphylococcus aureus

Cholera Mild gastroenteritis Diarrhea

Neurotoxin botulism Cholera

Black tea Catechins, theaavins

Friedman (2007) Friedman (2007)

Mycotoxicosis Ochratoxins Mycotoxicosis

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

Aspergillus niger Aspergillus parasiticus

Musyimi et al. (2008) Davidson and Naidu (2000)

Mint oil Thyme oil Cilantro oil Oregano oil Rosemary

Winter savory (Satureja montana) EO

Food-borne bacteria and improve quality

Carraminana et al. (2008)

Yes Yes (+++) Yes (+)

Dairy Mozzarella cheese Semi-skimmed milk Soft cheese

Listeria monocytogenes Listeria monocytogenes Listeria monocytogenes

Yes (+) Yes (+) From 1.0 ll g1(+)

Burt (2004) Burt (2004) Burt (2004)

(continued on next page)

1208 Table 4 (continued) Food group Yoghurt EO or component

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

Bacterial species Streptococcus thermophilus

Reference Burt (2004)

Tzatziki (yogurt and cucumber salad) Butter Dairy industries

Salmonella enteritidis Antioxidant Starter cultures and related food spoilage

Burt (2004) Ozkan et al. (2007) Viuda-Martos et al. (2008)

Rice Boiled rice Boiled rice Rice

Carvacrol Sage oil Ocimum basilicum

Yes (+++) No Yes

Burt (2004) Burt (2004) Lopez et al. (2008)

Fruit Kiwifruit Honeydew melon

Carvacrol, cinnamic acid Carvacrol, cinnamic acid

Natural ora Natural ora

Yes (+++) Yes (0+)

Burt (2004) Burt (2004)

Yes (+++) Yes (0+)