Food Control 21 (2010) 1199–1218
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
a
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 r t i c l e
i n f o
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
a b s t r a c t
Herbs and spices containing essential oils (EOs) in the range of 0.05–0.1% 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.
Ó 2010 Elsevier Ltd. All rights reserved.
Contents
1.
2.
3.
4.
5.
6.
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 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
* 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 Ó 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) 1199–1218
7.
Effectiveness determinations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
7.1.
Disc-diffusion method. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
7.2.
Drop-agar-diffusion method . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
7.3.
Broth microdilution method . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
7.4.
Direct-contact technique in agar . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Conclusions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
8.
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 artificial 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 benefits (Abou-taleb & Kawai, 2008; Fisher & Phillips, 2008;
Gaysinsky & Weiss, 2007; Gutierrez, Barry-Ryan, & Bourke,
2008a; Lopez-Malo vigil et al., 2005; Nazef, Belguesmia, Tani, Prevost, & Drider, 2008; Patrignani et al., 2008; Periago, Conesa, Delgado, Fernández, & Palop, 2006; Ponce, Roura, Del Valle, &
Moreira, 2008; Raybaudi, Mosqueda-Melgar, & Martin-Belloso,
2008;Yamamoto, Matsunaga, & Friedman, 2004).
Antimicrobials are used in food for two main reasons: (1) 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, O’Conner, Cotter, Hill & Ross,
2008; Lopez-Malo vigil et al., 2005; Martinez, Obeso, Rodriguez,
& Garcia, 2008; Murdak et al., 2007; Nazef et al., 2008; Oussalah,
Caillet, Salmiea, Saucier, & Lacroix, 2004; Pellegrini, 2003; Vagahasiya & Chanda, 2007).
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In addition to their flavoring 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 fields for food preservation and controlling pathogens and spoilage micro-organisms in food. However, technologies such as mild heat processing, modifiedatmosphere packaging, vacuum packaging and refrigeration are
not sufficiently 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 ml 1(Burt, 2004).
For example, combined mild heat treatment with addition of
cinnamon and clove EOs to apple cider significantly 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 fields, 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.
M.M. Tajkarimi et al. / Food Control 21 (2010) 1199–1218
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 flavor
and aroma. Plant extracts and spices, in addition to contributing to
taste and flavor, 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 first scientific 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 significant bacteriostatic properties (Burt,
2004; Ceylan & Fung, 2004; Gutierrez et al., 2008a; Jayaprakasha,
Negi, Jena, & Jagan Mohan Rao, 2007; Kwon, Kwon, Kwon, & Lee,
2008; Sofia, Prasad, Vijay, & Srivastava, 2007; Zaika, 1988).
Most spices have eastern origins; however, some of them 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 flavoring and
medicinal purposes (Ceylan & Fung, 2004).
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 flowers, 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 defined 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 field 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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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 fluid 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 efficacy 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 flavonoids, thiosulfinates,
glucosinolates and saponins.
Saponin and flavonoids are found in fruits, vegetables, nuts,
seeds, stems, flowers, tea, wine, propolis and honey. They commonly form a soapy lather after shaking in water. The antimicrobial activity of saponins and flavonoids 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). Thiosulfinates 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 flavor 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-
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M.M. Tajkarimi et al. / Food Control 21 (2010) 1199–1218
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 officinale), galangal (Alpinia galanga), turmeric (Curcuma longa), and fingerroot (Boesenbergia pandurata) extracts against Gram-positive
and Gram-negative pathogenic bacteria at 0.2–0.4% (v/v) for fingerroot and 8–10% (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 five
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 significant bacteriostatic/inhibition properties for patho-
genic and spoilage micro-organisms. Hydro-distilled EOs isolated
from the floral 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 purified 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; Rodríguez 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 flavor components. Source: Adapted from Ceylan and Fung (2004), Holley et al. (2005), and Naidu (2000a).
Category
Species
Plant part
Major flavor component
Bacterial inhibition (%)
Herbs
Basil, sweet (Ocimum basilicum)
Oregano (Origanum vulgare)
Rosemary (Rosmarinus offinicalis)
Sage (Salvia officinalis)
Thyme (Thymus vulgares)
Leaves
Leaves/flowers
Leaves
Leaves
Leaves
Linalool/methyl chavicol
Carvacrol/thymol
Camphor/1,8-cineole/borneol/camphor
Thujone, 1,8-cinole/borneol/camphor
Thymol/carvacol
<50
75–100
75–100
50–75
75–100
Spices
Allspice, pimento (Pimenta diocia)
Cinnamon (Cinnamonum zeylanicum)
Clove (Syzgium aromaticum)
Mustard (Brassica)
Nutmeg (Myristica fragrans)
Vanilla (Vanilla planifola, V. pompona, V.
tahitensis)
Berry/leaves
Bark
Flower bud
Seed
Seed
Fruit/seed
Eugenol/b-caryophyllene
Cinnamic aldehyde/eugenol
Eugenol
Allyl isothiocyanate
Myristicin/a-piene/Sabinene
Vanillin (4-hydroxymethoxybenzaldehyde)/pOH-benzyl methyl ether)
75–100
75–100
75–100
50–75
50–75
–
Oils
Olive oil
Tea-tree oil (Melaleuca alternifolia)
Fruit
Leaves
Oleuropein
Terpenoids
–
–
M.M. Tajkarimi et al. / Food Control 21 (2010) 1199–1218
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 0.05–0.1%
(500–1000 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 modifications (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 significant 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 flagellin highly significantly
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 influence 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 benefit 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 significant 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 25–100-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 efficacy 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 mustard’s 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-
1203
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 efficacy of EOs
against pathogenic micro-organisms (Lambert, Skandamis, Coote,
& Nychas, 2001).
Synergism between carvacrol and p-cymene, a very weak antimicrobial, might facilitate carvacrol’s 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 2–3 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
modified-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 findings 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 modified-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, 8–cineole (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 flavor caused by clove and tea tree
when used to protect against Escherichia coli O157:H7 and minimize
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M.M. Tajkarimi et al. / Food Control 21 (2010) 1199–1218
Table 2
Some reported sources of natural antimicrobials in plant within the last 10 years.
Plant name
Effective against
Reference
Coriander (Coriandum sativum), Oregano (Origanum vulgare),
Rosemary (Rosmarinus officinalis), Parsley (Petroselinum
crispum)
Gram-positive and Gram-negative bacteria,
including Listeria monocytogenes
Angioni et al. (2004), Ceylan and Fung (2004),
Daferera et al. (2000), El-Zemity, Radwan, El-Monam,
and Sherby (2008), Gutierrez et al. (2008a, 2008b),
Kim, Wei et al. (1995), Lopes-Lutz et al. (2008), and
Santos and Rao (2001)
Allipse (Pimenta dioica), Basil (Ocimum basilicum), Blue mallee
(Eucalyptus polybractea), Bay (Laurus nobilis), Caraway
seed (Carum carvil), Lemongrass (Cymbopogon citratus),
Lemon balm(Melissa officinalis), Marijoram (Origanum
majorana), Rosemary(Rosmarinus officinalis), and Sage
(Salvia officinalis)
Bacillus subtilis, Clostridium botulinum,
Escherichia coli, Listeria monocytogenes,
Salmonella typhimurium and Staphylococcus
aureus
Angioni et al. (2004), Burt (2004), Ceylan and Fung
(2004), Daferera et al. (2000), El-Zemity et al. (2008),
Greule and Mosandl (2008), Gutierrez et al. (2008a),
Gutierrez et al. (2008b), Kim , Wei et al. (1995),
Lopes-Lutz et al. (2008), Lopez-Malo vigil et al.
(2005), and Santos and Rao (2001)
Clove (Syzygium aromaticum) Sage (Salvia officinalis),
Cinnamon (Cinnamomum zeylanicum) and Marijoram
(Origanum majorana), Allipse (Pimenta dioica)
Pathogens such as Bacillus subtilis, Clostridium
botulinum, Escherichia coli, Listeria
monocytogenes, Salmonella typhimurium,
Staphylococcus aureus
Amiri et al. (2008), Burt (2004), Ceylan and Fung
(2004), Greule and Mosandl (2008), Gutierrez et al.
(2008a, 2008b), Ho, Wang, Wei, Lu, and Su (2008),
Kim, Wei et al. (1995), and Lopez-Malo vigil et al.
(2005)
Basil (Ocimum basilicum), Bay (Laurus nobilis), and
Lemongrass (Cymbopogon citratus)
Broad spectrum antibacterial effect against
Gram-positive and Gram-negative
pathogenic micro-organisms
Ceylan and Fung (2004) and Skocibusic et al. (2006)
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)
Staphylococcus spp.
Burt (2004), Greule and Mosandl (2008), Gutierrez
et al. (2008a, 2008b), Lopez-Malo vigil et al. (2005),
and Romeo et al. (2008)
Oregano (Origanum vulgare), Sage (Salvia officinalis), Thyme
(Thymus vulgaris) and Satureja hortensis L.
Staphylococcus aureus and Escherichia coli
Bousmaha-Marroki et al. (2007), Burt (2004), and
Razzaghi-Abyaneh et al. (2008)
Marjoram (Origanum majorana)
Alternative for synthetic preservatives
routinely used in the food industry
Mahmoud et al. (2007)
Cumin (Cuminum cyminum)
Bacillus cereus, Bacillus subtilis, Clostridium
botulinum, Listena monocytogenes,
Pseudomonas fluorescens, Salmonella
enteritidis, Staphylococcus aureus
Ceylan and Fung (2004)
Dill (Anethum graveolens)
Clostridium botulinum, Pseudomonas
aeruginosa, Staphylococcus aureus, Yersinia
enterocolitica
Ceylan and Fung (2004)
Fennel (Foeniculum vulgare)
Bacillus cereus, Clostridium botulinum,
Salmonella enteritidis, Staphylococcus aureus,
Yersinia enterocolitica
Ceylan and Fung (2004)
Garlic (Allium vineale)
Broad spectrum antibacterial effect against
Gram-positive and Gram-negative
pathogenic micro-organisms
Ceylan and Fung (2004)
Mint (Mentha piperita)
Broad spectrum antibacterial effect against
Gram-positive and Gram-negative
pathogenic micro-organisms
Ceylan and Fung (2004)
Onion (Allium cepa)
Escherichia coli, Salmonella typhimurium,
Shigella dysenteriae, Staphylococcus aureus
Ceylan and Fung (2004)
off flavor 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).
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. Review of some findings of in vitro experiments
Bacillus sp. were inhibited by: guarana extract (Majhenic,
Skerget, & Knez, 2007), EOs of Syzygium gardneri leaves (Raj,
George, Pradeep, & Sethuraman, 2008), supercritical fluid 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 fischeri (John
et al., 2008), EOs of the flower 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,
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 findings 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-
5.2. Bacillus sp.
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M.M. Tajkarimi et al. / Food Control 21 (2010) 1199–1218
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
Adverse
effects
Inhibitors
References
Bacillus cereus
Food
poisoning;
emesis
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
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 flavanols, 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
Campylobacter jejuni
Food
poisoning;
diarrhea
Black and green tea, cinnamaldehyde and carvacrol
Friedman (2007), Arques et al. (2008), and
Ravishankar, Zhu, Law, Joens, and Friedman (2008)
Escherichia coli
Food
poisoning;
diarrhea
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) films 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.
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)
Listeria monocytogenes
Food
poisoning;
listeriosis
Tea, pure essential oils, [Oregano in whey protein isolate
(WPI) films 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
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
Tuberculosis
Catechins, Bersama engleriana (Melianthaceae)
Friedman (2007), Kuete et al. (2008)
Pseudomonas aeruginosa
Food spoilage Tea extract, [Milk protein-based edible films 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 flavanols, 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
Pseudomonas fluorescens
Food spoilage Teas, [Milk protein-based edible films containing
oregano, 1.0% (w/v) pimento, or 1.0% oregano
pimento(1:1)], tannins, polymers of flavanols
Shigella spp. Tea
Diarrhea
Friedman (2007), Oussalah et al. (2004), and Yilmaz
(2008)
Tea, Bersam engleriana(Melianthaceae), tannins,
Arques et al. (2008), Friedman (2007), Kuete et al.
polymers of flavanols, 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
M.M. Tajkarimi et al. / Food Control 21 (2010) 1199–1218
Table 3 (continued)
Organism
Adverse
effects
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) films 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
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
Food
poisoning
Catechins
Friedman (2007)
Staphylococcus aureus
Food
poisoning;
infection
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)
films containing at 2% level, garlic essential oil at 3% and
4%], dried garlic powder, commercial garlic products,
clove, mustard, rosemary (Rosmarinus officinalis), lemon
balm (Melissa officinalis), sage (Salvia officinalis), 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
flavanols, lemongrass and bay; certain combinations of
carvacrol- thymol, citral, linalool and vapor, methanol and
acetone extracts of 14 plants belonging to different
families
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
Cholera
Tea extract
Arques et al. (2008)
V. parahaemolyticus
Mild gastroenteritis
Basil, clove, garlic, horseradish, marjoram, oregano,
rosemary, thyme, cassia bark-derived substances
Kong et al. (2007) and Yano et al. (2006)
Yersinia enterocolitica
Diarrhea
Teas, pure essential oils
Friedman (2007), Lopez et al. (2007)
Neurotoxin
botulism
Black tea
Friedman (2007)
Cholera
Catechins, theaflavins
Friedman (2007)
Mycotoxicosis
Pure essential oils, leaf oleoresin, leaf volatile oil,
eugenol, bark volatile oil, bark oleoresin, Ecinnamaldehyde, cassia bark-derived substances
Kong et al. (2007) and Lopez et al. (2007)
Aspergillus niger
Ochratoxins
Methanol extract of Aspilia mussambicensis
(Compositae)
Musyimi et al. (2008)
Aspergillus parasiticus
Mycotoxicosis
Thymol
Davidson and Naidu (2000)
Toxins
Botulinum
Cholera
Molds
Aspergillus flavus
Inhibitors
Wang, Chen, & Fu, 2007), specific 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 0.1–1.0% 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 fischeri (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 (Sofia et al.,
2007).
References
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 minutiflorum with a capacity as a food
preservative showed a variety of antimicrobial effects against
Campylobacter jejuni (Aslim & Yucel, 2007). The ciprofloxacin
resistance of Campylobacter strains has been shown to be
strongly diminished by application of EO of Origanum minutiflorum (Aslim & Yucel, 2007).
1207
M.M. Tajkarimi et al. / Food Control 21 (2010) 1199–1218
Table 4
Some studies regarding application of EOs or their components in-food studies conducted in the past 10 years.
Food group
EO or component
Bacterial species
Inhibitory effect
Reference
Clove oil , eugenol and coriander, oregano,
thyme oils, encapsulated rosemary EO,
clove and tea tree
Listeria monocytogenes,
Aeromonas hydrophila,
Escherichia coli O157:H7
Yes (+++)
Burt (2004) and Moriera et al.
(2007)
Fried meat
Oregano and thyme, oregano with
marjoram and thyme with sage
B. cereus and P. aeruginosa,
Escherichia coli O157:H7 and
Listeria monocytogenes
Yes (+)
Du and Li (2008)
Ground beef
Chinese cinnamon and winter savory EOs
Pathogenic micro-organisms
Yes (increased radiosensitivity)
Turgis et al. (2008)
Meat and poultry
Meat
Meat
EOs and nisin
Listeria monocytogenes
Yes
Solomakos et al. (2008)
Meat surfaces
Oregano, pimento, or oregano:pimento
Escherichia coli O157:H7 or
Pseudomonas spp.
Yes
Mosqueda-Melgar et al. (2008a,
2008b), and Oussalah et al. (2004)
Fresh sausage
Marjoram (Origanum majorana L.) EO
Several species of bacteria
Yes
Burt (2004)
Chicken
Eugenol
Listeria monocytogenes,
Aeromonas hydrophila,
Yes (+++++)
Burt (2004)
Chicken
Sage oil
Bacillus cereus, Staphylococcus
aureus, Salmonella typhimurium
No
Burt (2004)
Chicken
Oregano
Increase shelf life
Yes (with modifiedatmosphere
packaging)
Chouliara et al. (2007)
Pate
Mint oil
Listeria monocytogenes,
Salmonella enteritidis
No
Burt (2004)
Minced pork
Thyme oil
Listeria monocytogenes
No
Burt (2004)
Vacuum-packed ham
Cilantro oil
Listeria monocytogenes
No
Burt (2004)
Vacuum-packed
minced pork
Oregano oil
Clostridium botulinum spores
No
Burt (2004)
Liver pork sausage
Rosemary
Listeria monocytogenes
Yes (encapsulated
has more effect than
standard)
Hayouni, Chraief et al. (2008)
Minced pork
Winter savory (Satureja montana) EO
Food-borne bacteria and
improve quality
Yes (in combination
with other
techniques)
Carraminana et al. (2008)
Fish
Cooked shrimp
Thyme oil, cinnamaldehyde
Pseudomonas putida
Very slight
Burt (2004)
Red grouper fillet,
cubed
Carvacrol, citral, geraniol
Salmonella typhimurium
Yes (+++)
Burt (2004)
Cod fillets
Oregano oil
Photobacterium phosphoreum
Yes (+)
Burt (2004)
Salmon fillets
Cod’s roe salad
Oregano oil
Mint oil
Photobacterium phosphoreum
Salmonella enteritidis
No
Yes (+++)
Burt (2004)
Burt (2004)
Coated semi-fried
tuna slices
Eugenol and linalool
Increased shelf life
Yes
Naidu (2000a)
Fresh-water fish
Wild-thyme hydrosol
Increased shelf life, preservative
effect
Yes
Oral et al. (2008)
Lightly salted
cultured sea
bream (Sparus
aurata) fillets
Oregano
Increased shelf life, antioxidant
activity
Yes
Goulas and Kontominas (2007)
Carp fillets
Carvacrol + Thymol
Four times increased shelf life
Yes
Mahmoud, Kawai, Yamazaki,
Miyashita, and Suzuki (2006)
Carp
Thymol, carvcarol and cinnamaldehyde
Increased shelf life
Yes (+++)
Mahmoud et al. (2004)
Carp
Allyl isothiocyanate, carvacrol,
cinnamaldehyde, citral, cuminnaldehyde,
eugenol, isoeugenol, linalool and thymol
Increased shelf life
Yes (+)
Mahmoud et al. (2004)
Dairy
Mozzarella cheese
Clove oil
Listeria monocytogenes
Yes (+)
Burt (2004)
Semi-skimmed milk
Carvacrol
Listeria monocytogenes
Yes (+)
Burt (2004)
Soft cheese
DMC Base Natural preservative
comprising 50% EOs of rosemary, sage and
citrus
Listeria monocytogenes
From 1.0 ll g
1
(+)
Burt (2004)
(continued on next page)
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M.M. Tajkarimi et al. / Food Control 21 (2010) 1199–1218
Table 4 (continued)
Food group
EO or component
Bacterial species
Inhibitory effect
Reference
Yoghurt
Clove, cinnamon, cardamom, peppermint
oil
Streptococcus thermophilus
Yes (Mint oil +,
Cardamom, clove:
++, Cinamon:+++)
Burt (2004)
Tzatziki (yogurt and
cucumber salad)
Butter
Mint oil
Salmonella enteritidis
From 1.5%v/w ++
Burt (2004)
Satureja cilicica essential oil
Antioxidant
Yes
Ozkan et al. (2007)
Dairy industries
Oregano, thyme, rosemary, sage, cumin
and clove
Starter cultures and related food
spoilage
Yes
Viuda-Martos et al. (2008)
Vegetables
Lettuce, romaine
Thyme oil
E. coli O157:H7
Yes (+)
Burt (2004)
Carrots
Thyme oil
E. coli O157:H7
Yes (+++)
Burt (2004)
Lettuce, iceberg
green
Basil methyl chaviol (BMC)
Natural flora
Yes (++)
Burt (2004)
Eggplant salad
Oregano oil
E. coli O157:H7
Yes (++)
Burt (2004)
Alfalfa seeds
Cinnamaldehyde, thymol
Salmonella spp., six serotypes
Yes (50 °C: +, 70 °C:
0)
Burt (2004)
Rice
Boiled rice
Carvacrol
Natural flora
Yes (+++)
Burt (2004)
Boiled rice
Sage oil
Bacillus cereus, Staphylococcus
aureus, Salmonella typhimurium
No
Burt (2004)
Rice
Ocimum basilicum
Three stored-rice pests
(Sitophilus oryzae, Rhyzopertha
dominica and Cryptolestes
pusillus)
Yes
Lopez et al. (2008)
Fruit
Kiwifruit
Carvacrol, cinnamic acid
Natural flora
Yes (+++)
Burt (2004)
Honeydew melon
Carvacrol, cinnamic acid
Natural flora
Yes (0+)
Burt (2004)
5.4. Clostridium perfringens
5.6. L. monocytogenes
Clove EOs have an inhibitory effect against Clostridium perfringens at 0.4% (v/w) concentration (Davidson & Naidu, 2000).
Rosmarinus officinalis 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 0.5–0.7 w/v and were bacteriostatic at 0.5–1.0% concentration; and borneol extracted from
sage and rosemary had inhibitory effect against L. monocytogenes
at 0.02–0.05% 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 flowers of Salvia
reuterana (Lamiaceae) (Esmaeili et al., 2008), linalool vapor of bergamot and linalool oils (Fisher & Phillips, 2008),water-distilled EO
from leaves and flowers of Micromeria nubigena H.B.K. (Lamiaceae)
(El-Seedi et al., 2008), hydro distillation leaf oil of Cinnamomum
chemungianum (Raj et al., 2008), Rosmarinus officinalis 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 0.12–0.25% 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 flower 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 (Sofia et al., 2007).
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. flavus; 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 flowers 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 Aflatoxins production
has been inhibited by Thymus vulgari and Citrus aurantifolia,
whereas Mentha spicata L., Foeniculum miller, Azadirachta indica A.
M.M. Tajkarimi et al. / Food Control 21 (2010) 1199–1218
Juss, Conium maculatum and Artemisia dracunculus has only inhibited the fungal growth, while Carum carvi L. has controlled aflatoxin 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 flowering stages) and flowers 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, specifically 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 flowers 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 fischeri (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 fluorescens (Raj et al., 2008).
Guarana extract (Majhenic et al., 2007) and leaves, bark and fruits
of Neolitsea fischeri (John et al., 2008) were active against Pseudomonas fluorescens.
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 flavoring, Zataria multiflora 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 0.12–0.25% v/v
concentration (Davidson & Naidu, 2000), leaves bark and fruits of
Neolitsea fischeri (John et al., 2008, hydro-distilled EOs of fresh
leaves and mature fruits of Pittosporum viridulum (John et al.,
2007).
1209
According to a study on Mueller–Hinton (MH) Agar and MH
broth, cloves showed antimicrobial effect against Shigella sonnei,
Shigella flexneri 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 flowers 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 officinalis oil (Gachkar et al., 2007); EOs of
Zataria multiflora 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 0.4–0.6% w/v concentration; clove EOs at 0.4% (v/
w) concentration; EOs from thymol and carvacrol 5%, 10%, 15%,
and 20% concentration, EOs from thymol and carvacrol at 175–
225 lg/ml concentration; cinnamic aldehyde and eugenol 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 0.12–0.25% 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 fischeri (John et al., 2008), water-distilled EOs from leaves and flowers
of Micromeria nubigena H.B.K. (Lamiaceae) (El-Seedi et al., 2008),
Curcuma domestica and Curcuma viridiflora at ratios of 20/15 (Chen
et al., 2008), anzer tea’s EOs (Sekeroglu et al., 2007), EOs of the
flower 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 flavanols (Yilmaz, 2006), and Curcuma
domestica and Curcuma viridiflora 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 flowering stages) and flowers 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
33–35 bacteria, yeasts and molds (Davidson & Naidu, 2000).
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M.M. Tajkarimi et al. / Food Control 21 (2010) 1199–1218
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 effluent, 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
1.25–5 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 flavus) (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 floral 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 (Sofia 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 flora in meat products. However, mustard, cilantro, mint and sage oils were less effective or ineffective
(Burt, 2004). A 5–20 ll g 1 level of eugenol and coriander, clove,
oregano and thyme oil inhibits growth of L. monocytogenes, Aeromonas hydrophila and autochthonous spoilage flora 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 officinalis 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 fields, irradiation,
or packaging under a modified 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 significantly reduced oxidation, while the heat treatment and storage time significantly affected the antioxidant activity
of the meat (Fasseas, Mountzouris, Tarantilis, Polissiou, & Zervas,
2007). Milk protein-based edible films containing oregano, pimento,
or oregano/pimento were effective against Escherichia coli O157:H7
or Pseudomonas sp. on meat surfaces (Mosqueda-Melgar et al.,
2008a; Mosqueda-Melgar et al., 2008b; Oussalah et al., 2004).
Chlorophyll-containing films were tested against 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 films and coatings (López-Carballo, Hernández-Muñoz, 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 films and
coating applications successfully reduced Staphylococcus aureus
and L. monocytogenes in cooked frankfurter (López-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 fluorescens and Lactobacillus sake) in modified 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
M.M. Tajkarimi et al. / Food Control 21 (2010) 1199–1218
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 fish, 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 fishes. For example, oregano oil is more effective
against the spoilage organism Photobacterium phosphoreum on
cod fillets than on salmon, which is a fatty fish. Oregano oil is more
effective than mint oil in/on fish, even in fatty-fish dishes. Application of EOs on the surface of whole fish or as coating for shrimps
inhibited Salmonella Enteritidis, L. monocytogenes and natural
spoilage flora (Burt, 2004; Hayouni & Chraief et al., 2008).
There is significant preservative and increased shelf-life effects
of wild thyme (Thymus serpyllum), about 15 to 20 days with freshwater fish (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 fillets 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 fillets, 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 influence 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
1211
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 flora 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 final 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 five 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 flora on kiwi fruit (pH 3.2–3.6) was effectively inhibited
by carvacrol and cinnamaldehyde but less effectively on honeydew
melon (pH 5.4–5.5), 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 microflora 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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M.M. Tajkarimi et al. / Food Control 21 (2010) 1199–1218
6.7. Animal feed
7. Effectiveness determinations
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).
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 emulsifier and basic test method (Sofia et al., 2007).
Antimicrobial activity in most experiments has been quantified on
two bases, MIC and MBC (minimum bactericidal concentration),
which is presumably greater than the MIC. MIC is defined in different
terms; some of them are ‘‘lowest concentration resulting in maintenance or reduction of inoculum’s 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
Method
Bacillus cereus, Pseudomonas aeruginosa and
Escherichia coli
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
Arques et al.
(2008)
Escherichia coli and Staphylococcus aureus
Direct contact assay method in order to define Minimum
Inhibitory Concentration (MIC).
Becerril et al.
(2007)
Escherichia coli and Staphylococcus aureus
Modified disc-diffusion method originated from Jorgensen, Four strains of Tunisian
Turnidge, and Washington (1995)
Chrysanthemum species
Ben Sassi et al.
(2008)
Bacillus cereus
Luria–Bertani (LB) agar plates
Tea flavonoids
Friedman
(2007)
Bacillus cereus, Escherichia coli O157:H7, Listeria
monocytogenes and Salmonella enterica
The modified bactericidal assay described previously by
Friedman, Henika, Levin, Mandrell, Kozukue (2006)
Extract of oregano leaves with added Friedman,
garlic juice and oregano oil
Henika, Levin,
& Mandrell
(2007)
Escherichia coli and Pseudomonas fluorescens
Well-diffusion test described by Kim, Marshall et al.
(1995)
Different ethanol extracts of soices
honeysuckle, Scutellaria, Forsythia
suspensa (Thunb), cinnamon,
rosemary and clove oil
Gram-negative, Gram-positive bacteria and molds Modified vapor diffusion test which is explained in detail
by Isidorov and Vinogorova (2005)
Inhibitors
Cinnamon or oregano
Reference
Kong et al.
(2007)
Three commercially available
Lopez et al.
essential oils (EOs) cinnamon ,thyme, (2007)
and oregano
Escherichia coli, Bacillus cereus and Pseudomonas
fluorescens
Method described by Janssen, Scheffer, and Baerheim
Guarana seed extract
Svendsen (1987) and Vagi, Simandi, Suhajda, and Hethelyi
(2005)
Majhenic et al.
(2007)
Bacillus cereus, Pseudomonas aeruginosa and
Escherichia coli
Pit and disc methods according to Rajakanuna, Harris, and Methanol extract of Aspilia
Towers (2002)
mossambicensis (Compositae)
Musyimi et al.
(2008)
Campylobacter jejuni
Different concentrations of main constituents of plantderived cinnamon and oregano oils, in sterile phosphatebuffered saline
Cinnamaldehyde and carvacrol
Ravishankar
et al. (2008)
Escherichia coli
Modified method explained by Friedman, Henika, and
Mandrell (2002), Friedman, Henika, Levin, and Mandrell
(2004)
Oregano oil/carvacrol; cinnamon oil/ Rojas-Grau
cinnamaldehyde; and lemongrass oil/ et al. (2007)
citral
Bacillus cereus, Bacillus subtilis Staphylococcus
aureus, Escherichia coli, Salmonella typhi and
Pseudomonas aeruginosa
Growth zone-inhibition developed method described by
Davidson and Parish (1989)
Volatile oils and oleoresin of
Cinnamomum zeylanicum Blume
(leaf and bark)
Singh et al.
(2007)
Salmonella enteritidis, Escherichia coli O157:H7,
Listeria monocytogenes and Staphylococcus
aureus
Zone of inhibition assay on solid medium
Oregano, rosemary and garlic
essential oils
Seydim and
Sarikus (2006)
Escherichia coli, Staphylococcus aureus and Bacillus Disc-diffusion technique
cereus
Six Indian spice extracts: clove,
Winward et al.
cinnamon, mustard, garlic, ginger and (2008)
mint
Escherichia coli
Agar plate method
Cabbage juices
Salmonella typhimurium, Pseudomonas aeruginosa,
Escherichia coli, Staphylococcus aureus, Bacillus
cereus, Bacillus subtilis and Salmonella
typhimurium
Agar disc-diffusion method (Nair, Kalariya, & Chanda,
2005)
Methanol and acetone extracts of 14 Vagahasiya
plants belonging to different families and Chanda
(2007)
Vibrio parahaemolyticus and Escherichia coli
Screening growth or survival of these two bacteria at
different temperatures in nutrient-rich medium and
defined pH
18 Plant species
Tolonen et al.
(2004)
Yano et al.
(2006)
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M.M. Tajkarimi et al. / Food Control 21 (2010) 1199–1218
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 significant decrease in
inoculum’s viability (>90%).” MBC is defined 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
0.05–5 ll m 1 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 modifications 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 defini-
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 efficacy 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 filter 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).
Identification of antimicrobial activity is significantly 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 definitions, 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
Escherichia coli
Well/cupd
Staphylococcus aureus
Disc
Well/cup
Cinnamon
0.5
1
2
3
10.3 ± 0.5
11.0 ± 0.0
11.3 ± 0.5
12.0 ± 0.0
–
10 ± 0
11.6 ± 0.5
13.3 ± 0.5
8.0 ± 0.0
10.0 ± 0.0
12.3 ± 0.5
14.3 ± 0.5
–
10.6 ± 0.5
12.6 ± 0.5
14 ± 1
–
–
10.0 ± 0.0
11.6 ± 0.5
–
10 ± 0
10.6 ± 0.5
12.3 ± 0.5
Clove
0.5
1
2
3
10.3 ± 0.5
11.3 ± 0.5
12.6 ± 0.5
16.0 ± 0.0
–
14.6 ± 0.5
23.6 ± 0.5
25.6 ± 0.5
11.6 ± 0.5
13.3 ± 0.5
15.6 ± 0.5
19.3 ± 0.5
16.3 ± 0.5
17.3 ± 0.5
20.3 ± 0.5
23.3 ± 0.5
–
–
12.6 ± 0.5
16.3 ± 0.5
–
18.3 ± 0.5
23.6 ± 0.5
25.6 ± 0.5
Garlic
0.5
1
2
3
11.6 ± 0.5
12.6 ± 0.5
14.0 ± 0.0
14.3 ± 0.5
–
–
–
10.6 ± 0.5
10.0 ± 1.0
10.0 ± 0.0
11.3 ± 0.5
12.3 ± 0.5
10.3 ± 0.5
12.3 ± 0.5
13.0 ± 1.0
13.0 ± 0.0
10.6 ± 0.5
12.0 ± 0.0
12.3 ± 0.5
14.0 ± 1.0
–
–
10.3 ± 0.5
11.6 ± 0.5
Ginger
0.5
1
2
3
9.6 ± 0.5
10.3 ± 0.5
11.0 ± 0.0
11.6 ± 0.5
–
–
10.3 ± 0.5
11.3 ± 0.0
9.3 ± 0.5
10.3 ± 0.5
10.6 ± 0.5
11.3e ± 0.5
–
–
10.0 ± 0.0
11.3 ± 0.5
10.6 ± 1.1
11.3 ± 0.5
13.0 ± 1.0
14.6 ± 0.5
–
–
10.6 ± 0.5
12.3 ± 0.5
Mint
0.5
1
2
3
11.3 ± 0.5
14.6 ± 1.1
14.6e ± 0.5
18.3e ± 1.1
13.3 ± 0.5
14.0 ± 0.0
14.6e ± 0.5
16.6e ± 0.5
–
13.3 ± 0.5
15.0e ± 1.0
16.3e ± 0.5
–
–
8.6e ± 0.5
9.3e ± 0.5
12.6 ± 0.5
14.3 ± 0.5
15.0e ± 1.0
17.3e ± 0.5
13.3 ± 0.5
14.6 ± 0.5
26.6e ± 0.5
27.6e ± 0.5
Mustard
0.5
1
2
3
–
10.3 ± 0.5
11.6 ± 0.5
15.6 ± 0.5
–
9.6 ± 0.5
10.3 ± 0.5
11.3 ± 0.5
11.6 ± 0.5
19.3 ± 0.5
21.6 ± 0.5
25.6 ± 0.5
8±0
12.6 ± 0.5
14.6 ± 0.5
19.3 ± 0.5
10.3 ± 0.5
11.6 ± 0.5
14.3 ± 0.5
16.0 ± 1.0
–
–
8.3 ± 0.5
9.6 ± 0.5
Differences between different concentrations within a spice found to be significant 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.
Disc
Well/cup
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M.M. Tajkarimi et al. / Food Control 21 (2010) 1199–1218
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 difficulties 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 flavoring
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 flavor due to application of antimicrobial components are a major issue. However, flavor 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 films 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 flavorings 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
flavoring 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 define 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
modified-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.
M.M. Tajkarimi et al. / Food Control 21 (2010) 1199–1218
Evaluation of new preservatives such as natural antimicrobials
in food, evaluating food structure, composition and interaction between natural microflora 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.
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