Antimicrobial Activity of Spices

ANTIMICROBIAL ACTIVITY OF SPICES’
ERDOGAN CEYLAN and DANIEL Y. C. FUNG’
Food Science Institute

Kansas State University
Manhattan, Kansas 66506
Accepted for Publication March 29, 2004
ABSTRACT
Many of the spices and herbs used today have been valued for their
antimicrobial effects and medicinal powers in addition to their flavor and
fragrance qualities. Most of the foodbome bacterial pathogens examined were
sensitive to extractsfrom plants such as cinnamon, clove, garlic, mustard, onion
and oregano. me antimicrobial compounds in spices and herbs are mostly in the
essential oil fraction. The Gram-positive bacteria were more sensitive to the
antimicrobial compounds in spices than Gram-negarive bacteria. The extent of
sensitivity varied with the strain and environmental conditions imposed. Certain
spices can have a direct effect on the rate of fermentation by stimulating acid
production in starter cultures. Phenols, alcohols, aldehydes, ketones, ethers and
hydrocarbons have been recognized as major antimicrobial components in
spices. m e antimicrobial activity and modes of actions of spices and their major
antimicrobial components are reviewed.
INTRODUCTION
Spices are desirable food ingredients to create and explore new tasty
products. Understanding and analyzing their properties, and developing new
methods and instruments to study them are critical for today’s food product
manufacturing (Madsen and Grypa 2000). There is no particular definition of
spices because it is very difficult to define what a spice is compared to a herb.
Spices are derived from different parts of the plants such as cardamom from
seed, bay leaf from leaf, clove from flower bud, pepper from fruit, cinnamon
I This material is based upon work supported by the Cooperative State Research Education, and
Extension Service, the United States Depament of Agriculture, under agreement No. 93-34211-
8362. This is contribution number 03-131J Kansas Agricultural Experiment Station, Manhattan,
KS 665064008.
* Correspondence to: 225 Call Hall, Kansas State University, Manhattan, Kansas 66506. TEL: (785)
532-5654; FAX: (785) 532-5681; EMAIL: dfungQoznet.ksu.edu
Journal of Rapid Methods and Automation in Microbiology 12 (2004) 1-55. All Rights Resewed.
OCopyrighr 2004 by Food & Nutrition Press, Inc.. Trurnbull, Connecticut. 1
2 E. CEYLAN and D.Y.C. FUNG
from bark or ginger from rhizome. Many spices require tropical or subtropical
climates to grow. Herbs are soft-stemmed plants and both fresh and dried forms
of leaves and flowering tops are used for the seasoning of foods (Lewis 1984).
The smell of the original spice oil is dependent on its composition. In many
cases no single component has the characteristic smell. A complex mixture
influences the overall odor quality. Some parts of the volatile oils of spices are
lost during the processing of foods. The important compounds are not so volatile
and are entrapped by fat and proteins in the food. In addition to their aroma and
pungency factors, spices contain many different compounds such as fat and resin
to give the natural flavor of spices. Some spices like paprika, turmeric and
saffron have the advantage of not only giving a flavor but also giving attractive
colors to foods (Lewis 1984).
Spices consumed in small quantities contain little or no nutritive values
compared to vegetables that contain high amounts of protein, carbohydrates, fat,
starch, fiber, minerals and different vitamins (Farrell 1985). However, spices
supply secondary compounds that have medicinal, antioxidant and antimicrobial
effects. Spices contain variable amounts of protein, fat, carbohydrate, small
quantities of vitamins (e.g., carotene, thiamine, riboflavin and niacin) and
inorganic elements (calcium, magnesium, manganese, phosphorous, potassium,
chlorine, copper, iron, sodium and zinc). Some spices also contain fatty acids,
starch, sugars, cholesterol and fiber (Lewis 1984; Farrell 1985; h u n g and
Foster 1996). Spices are not used only in countries where the plants grow.
However, the proportion of the use of spices is higher in countries where spices
grow (Billing and Sherman 1998).
Use of spices in cooking is the oldest form of aromatherapy that stimulates
gastric secretion and creates appetites, stimulates the body, creates positive
moods, relieves cold symptoms and respiratory problems, and eases muscle
pains. The active components in spices are considered as powerful tools to
create a state of wellness such as stimulate production of enzymes that detoxify
carcinogens, inhibit cholesterol synthesis, block estrogen, lower blood pressure
and prevent blood clotting (Uhl2000). Many herbs have antioxidant properties
and reduce the deterioration of color of meat by reducing the degree of oxidation
of fat in the meat (Lewis 1984).
There is no common method to classify spices. However, the most common
classification (Clark 1970) is based on the flavor and color, i.e., hot (pepper),
pungent (garlic), aromatic (cinnamon, clove), coloring (turmeric), and
herbaceous (rosemary, sage). Spices are also classified according to their taste
such as sweet, spicy, sour, bitter and astringent. The aroma is due to volatile
essential oils of different chemical compositions such as terpenes,
sesquiterpenes, aldehydes, ketones, phenols, esters, ethers, oxides, etc. (Lewis
1984).
ANTIMICROBIAL ACTIVITY OF SPICES 3
Extracts of plants, spices and herbs play an important role in promoting

human health by their anticancer, antioxidative and anti-inflamatory properties.
Flavonoids from tea beverages act as free radical-scavengers and antioxidants
(Wiseman er al. 1997). Anthocyanins and flavonoids from teas and cherries
possess antiallergic, antiviral, anticancer and anticarcinogenic properties, and
prevent cardiovascular diseases and aging (Balentine et al. 1999). Components
in spices also possess colorant, bioactive (i.e., antioxidant and antimicrobial),
acidulant and sweetener effects (Chang er al. 1977; Pszczola 1999; Mansour and
Khalil 2000; Wang er al. 2000).
Essential oils (volatile oils) are distilled parts of spices by mostly steam, and
also by cold, dry and vacuum distillation methods (Giese 1994a). Oleoresins,
solvent extracts of spices, contain both volatile and nonvolatile fraction of spices
(Farrell 1985).
HISTORY
Spices are primarily condiments used in cooking in modem life but in

ancient times they were used as basic ingredients of incense, embalming
preservatives, ointments, perfumes, antidotes against poisons, cosmetics and
medicines, and were valued as condiments in cooking to a limited extent. Spices
were used as condiments in food for the first time, in the first century AD in
Rome. Medieval Europeans used spices to flavor the drab and partially
decomposed food, to provide fragrance and to mask noxious odors. The demand
for spices played an important role in world history; which stimulated the
exploration of the globe, the discovery of continental America by Europeans,
and the initiation of trade and cultural interaction between the countries of East
and West (Rosengarten 1969).
The first recorded use of spices was dated from the Pyramid Age in Egypt
(2600 BC). Onions were fed to laborers as medicinal herbs to preserve their
health during construction of pyramids. The spices and herbs used today as
condiments such as anise, caraway, cassia, coriander, fennel, cardamom,
onions, garlic, thyme, mustard, sesame, fenugreek, saffron, and poppy seed
were used in medicine, cosmetics, cooking and embalming. In China, the first
authentic record of the use of cassia was found in the Ch’u Ssu (Elegies of Chu)
in the fourth century BC. The great philosopher Confucius (551-479 BC)
mentioned the use of ginger in his Analects. Excavations in the Indus Valley
show that spices and herbs have been used since the first millennium BC
(Rosengarten 1969).
In the ancient Greece, spices and herbs played an important role in medical
science and as condiments in food. They imported some Eastern spices such as
pepper, cassia, cinnamon and ginger, and also used spices and herbs grown in
the Mediterranean area such as anise, caraway, poppy seeds, parsley and
marjoram. Hippocrates (460-377 BC), the “Father of Medicine”, wrote many
treatise on medicinal plants and their use. The Greek philosopher and scientist
Theophrastus (327-287 BC), sometimes called the “Father of Botany”, wrote
two books, On Odors and An Enquiry into Plants, that gathered the botanical
information of spices and herbs (Rosengarten 1969).
The transportation of spices and other goods from East to West created
several ancient trade routes; the “Incense Route” and the “Silk Route”. High
demand and cost of spices in the Middle Ages encouraged the Europeans to find
the new routes to primarily spice growing regions in the Orient. Marco Polo,
Pedro Cabral, Vasco da Gama, Ferdinand Magellan, Christopher Columbus and
Hernando Cortes were the pioneers who established new routes for spice trading
(Parry 1969). The crucial role of spices in the countrys’ economy resulted in the
discovery of new lands, wars between countries, and raids of spice growing
countries (Farrell 1985; Parry 1969).
Although most of the spices came from the East, some popular spices were
introduced to Europe and Asia after discovering the New World. Chili peppers,
sweet peppers, allspice, annatto, chocolate, epazote, sassafras, and vanilla were
used by Aztecs, Mayans, and Incas to flavor their food and drinks, and for
medicinal purposes (Uhl 2000).
USE OF SPICES IN FOOD
Spices and herbs, aromatic vegetable materials, have long been used in
foods not only for their flavoring, but also for their medicinal and preservative
properties (Davidson el al. 1983). Spices also stimulate appetite by increasing
salivation, carminative action, and preserve the food by their antimicrobial and
antioxidant properties (Lewis 1984). More than 400 spices are used in the
different countries in the world. Since ancient times, spices and herbs have been
used for preventing food spoilage and deterioration, and for extending shelf-life
of food, as well (Nakatani 1994).
Spices are used to enhance the flavor and palatability of food. Billing and
Sherman (1998) evaluated several critical predictions in order to address the
question of why people use spices. The authors evaluated the prediction of the
use of 43 spices in 4,578 meat-based recipes from 36 countries. They concluded
that in hot climate countries the proportion of recipes with spices, number of
spices used in each recipe, total number of spices, and the use of most
antimicrobial spices were higher. Spices are used to enhance food flavor and
palatability. Countries with high mean annual temperature use numerous spices
compared to countries with low mean annual temperature. In hot climate
countries spices are more frequently used at higher amounts than cool climate
countries. Spices with strong antimicrobial activity such as garlic, onion,

capsicum, cinnamon, and cumin are used more frequently in countries with hot
climates than countries with cooler climates. Furthermore, hot country cuisines
and spicier cuisines have more antimicrobial potent against foodborne
microorganisms (Billing and Sherman 1998).
Billing and Sherman (1998) had two hypotheses about how people started
using spices. First, people who used spices, especially in hot countries, suffered
less from foodborne illnesses and stored their food for longer periods of time.
Second, adding spices changed the taste and flavor of food, and made it more
palatable and safe for consumption.
Billing and Sherman (1998) compared the antimicrobial properties of 30
different spices and summarized the antibacterial spectrum of each spice. All of
the spices evaluated inhibited the growth of some bacteria, 80% of spices
inhibited more than 50% of bacteria tested, 50% of spices inhibited more than
75% of bacteria tested, and 13%of spices inhibited all of bacteria tested (Table
1). The antibacterial spectrum of the most commonly used spices is given in
Table 2.
The amount of spice extracts used in food systems range from 0.05 to 0.1 74
(500 to 1000 ppm; Salzer 1982). Billing and Sherman (1998) calculated that
meat recipes contained roughly 0.25-3 .O g/kg of spices (250-3000 ppm).
Although many of the spice essential oils have antimicrobial effects against
bacteria less than 1000 ppm (Huhtanen 1980; Kivanc and Akgul 1986; Zaika
1988), some spices require higher concentration to exhibit antimicrobial effect.
TABLE 1 .
PROPORTIONAL INHIBITORY PROPERTIES OF SPICES AGAINST BACTERIAL
STRAINS TESTED'
Percent Bacterial Inhibition Spice
75-100% Garlic, onion, allspice, oregano, thyme, cinnamon,

tarragon, cumin, cloves, lemon grass bay leaf,
capsicums, and rosemary
50-75 % Marjoram, mustard, caraway, mint, sage, fennel,

coriander, dill, and nutmeg
Less than 50 % Basil, parsley, cardamom, pepper (black and white)

ginger, anise seed, celery seed, lemon, and lime
'Adapted from Billing and Sherman 1998.

TABLE 2.
ANTIMICROBIAL SPECTRUM OF SPICES AGAINST BACTERIAL SPECIES’
Spice Bacterial Species Bacterial Species Not References

Inhibited Inhibited
Allspice Bacillus subtilis None Hargreaves et al. 1975
Clostridium botulinum Hefnawy et al. 1993
Escherichia coli Huhtanen 1980
Listeria monocytogenes Shelef et al. 1980
Serratia marcescens
Basil A cinetobacter calcoaceticus Aeromonas hydrophila Deans and Ritchie 1987
Alcaligenes faecalis Bacillus subtilis
Beneckea narriegens Brevibacrerium linens
Citrobacterfreundii Brochothnx thermosphacta
Enterobacter aerogenes Clostndium sporogenes
Erwinia carotovora Escherichia coli
Flavobacterium suaveolens Lactobacillus planrarum
Klebsiella pneumoniae Micrococcus luteus
Leuconostoc cremoris Proteus vulgaris
Pseudomonas aeruginosa Staphylococcus aureus
Salmonella Pullorurn Streptococcusfaecalis
Serratia marcescens Yersinia enrerocolitica
Bay Leaves Actnetobaaer calcoacettcus Brevibactenum linens Akmg and Karapinar I986
Aeromonas hydrophila Clostndium sporogenes Beuchat 1994
Alcaligenes faecahs Micrococcus luteus Deans and Ritchie 1987
Bacillus subtilis Salmonella Typhimuriurn Hargreaves el al. 1975
Beneckea natnegens Streptococcusfaecahs Huhtanen 1980
Brochothm thermosphacta
Citrobacterfreundii
Clostndium botulinum
Enterobacter aerogenes
Erwinia carotovora
Eschenchia coli
Flavobactenum suaveolens
Klebsiella pneumoniae
Lactobacillus plantarum
Leuconosroc cremons
Proteus vulgaris
Pseudomonas aerugrnosa
Salmonella Pullorurn
Serratia marcescens
Staphylococcus aureus
Vibno parahaemolyticus
Yersinia enterocolitica
Table 2. continued
Inhibited Inhibited
Cinnamon Acinetobacter calcoaceticus Clostridrum sporogenes Azzouz and Bulleman 1982
Aeromonas hydrophila Enterobacter aerogenes Bayoumi 1992
Alcaligenes faecalis Pseudomonas aeruginosa Beuchat 1994
Bacillus anthracis Streptococcusfaecalis Deans and Ritchie 1987
Bacillus cereus El-Kady et al. 1993
Bacillus subtilis Ting and Deibel 1992
Beneckea natriegens Hargreaves el al. 1975
Brevibacterium linens Huhtanen 1980
Brochothrix thermosphacm Islam et al. 1990
Cztrobacterfreundii
Envinia carotovora
Escherichia coli
Flavobactenurn suaveolens
Lactobacillus bulgaricus lsmaiel and Pierson 1990a
Lactobacillus plantarum Shelef er al. 1984
Leuconostoc cremoris Zaika 1988
Listena monocytogenes
Micrococcus luteus
Proreus vulgaris
Pseudomonasjluorescens
Pseudomonas pyocyanea
Salmonella Paratyphi
Serratia mrcescens
Serratia rhadnii
Streptococcus nasik
Streptococcus thermophrlus
Yersrnia enterocolitica
Table 2. continued
Inhibited Inhibited
Clove Acinetobacter calcoaceticus Clostridium sporogenes Azzouz and Bullerman 1982
Aeromonas hydrophila Micrococcus (Sarcina) Bayoumi 1992
Bacillus anthracis Pseudomonaspyocyanea Beuchat 1994
Bacillus cereus Salmonella Paratyphi Briozzo et al. 1989
Bacillus subtilis Serratia rhadmi Deans and Ritchie 1987
Beneckea natnegens El-Kady et al. 1993
Cirrobacterfreundii Ting and Deibel 1992
Clostridium botulinum Farag et al. 1989b
Clostridiumperfnngens Hargreaves et al. 1975
Enterobacfer aerogenes Huhtanen 1980
Eminia caroiovora Isrnaiel and Pierson 1990a
Escherichia coli lay and Rivers I984
Flavobacterium suaveolens Ramadan et al. 1972
Klebsiella pneumoniae Shelef et al. 1984
Lactobacillus bulgaricus Stecchini et al. 1993
Lactobacillus plantarum Zaika 1988
Leuconostoc cremoris
Micrococcus luteus
Mycobacrerium phlei
Proreus morganii
Proteus vulgaris
Pseudomonas aeruginosa
Pseudomonas puorescens
Salmonella Enteritidis
Serratia marcescens
Streptococcusfaecalis
Streptococcus msik
Sireptococcus thermophilius
Cumin Aerobacter aerogenes Klebsiella pneumoniae Azzouz and Bullerman 1982

Bacillus anthracrs Pseudomonas pyocyanea El-Kady et al. 1993
Bacillus cereus Serratia rhadnii Farag et al. 1989b
Bacillus coagulans Hassan et al. 1989
Bacillus subtilis Hefnawy et al. 1993
Clostndium botulinum Huhtanen 1980
Enterobacier aerogenes Kivanc and Akgul 1986
Lactobacillus plantarum Kivanc et al. 1991
Table 2. continued
Inhibited Inhibited
Cumin Leuconosotoc mesenteroides Ramadan et al. 1972
(cont) Listena monocyfogenes Saxena and Vyas 1986
Micrococcus (Sarrina) Sherry et al. 1994
Proreus vulgans
Pseudomonasjluorescens
Serratia marcescens
Staphylococcus albus
Streptococcus nasik
Dill Acinefobacter calcoaceticus Alcaligenesfaecalis Deans and Ritchie 1987

Aerobacter aerogenes Beneckea natnegens Hargreaves et a1 1975
Aeromnas hydrophila Brochorhm thermosphacta Huhtanen 1980
Brevibactenum h e n s Clostndium botulinum Kivanc and Akgul 1986
Citrobacferfreundii Clostndium sporogenes Ramadan et al. 1912
Emerobacter aerogenes Lactobacillus plantarum
Envinia carotovora Leuconostoc cremons
Flavobanenum suaveolens Micracoccus lufeus
Klebsiella pneumoniae Salmonella Pullorum
Proreus vulgans Staphylococcusfaecalis
Pseudomonas aeruginosa Yersinia enlerocohtica
Serratia marcescens
Fennel Aerobacter aerogenes Alcaligenes faecalis Deans and Ritchie 1987

Bacillus cereus Beneckea natnegens Hargreaves et a1 1975
Bacillus subtilis Brevibactenum linens Huhtanen 1980
Cirrobacterfreundii Brochothm thermosphacta Kivanc and Akgul 1986
Emerobacter aerogenes Clostndium bofuhnum Ramadan et a1 1972
Erwinia carotovora Clostndium sporogenes
Flavobactenum suaveolens Klebsiella pneumoniae
Leuconosfoc cremoris hcrabacillus p l a n t a m
Proreus vulgaris Micrococcus luteus
Salmonella Enteritidis Yersinia enferocolitrca
Serratia marcescens
Table 2. continued
Inhibited Inhibited
Garlic Bacillus cereus None Abdou et al. 1972
Bacillus subtilis Beuchat 1994
Compylubacterjejuni El-Khateib and El-Rahman
Clostridiumperfnngens 1987
Enterobacier cloacae Ting and Deibel 1992
Enterococcusfaecalis Gandi and Ghodekar 1988
Enrerococcus faecium Hargreaves ei al. 1975
Escherichia coli Hef’nawy et al. 1993
Klebsiella aerogenes Hughes and Lawson 1991
Klebsrella pneumoniae Huhtanen 1980
Lactobacillus acidophilus lsrnaiel and Pierson 1990b
Luctobacillus plantarum Rees ei al. 1993
Listeria monocyiogenes Sat0 ei al. 1990
Pediococcuspentosaceus Sbelef 1984
Proteus mrrabilis
Proteus morganii
Proteus vulgaris
Pseudomonas fluorescens
Salmonella Dublin
Salmonella Typhimurium
Serratia marcescens
Siaphylococcus aureus
Siaphylococcus epidemidis
Streptococcus agalacirae
Vibrio mimicus
Vibrioparahaemolyticus
Yersinia enterocolitica
Lemongrass Bacillus ceretis Sireptococcusfaecaiis Onawunmi and Ogulana 1986

Bacillus subtilis Ramadan 1972
Escherichia coli
Staphylococcus auerus
Mint Acinetobacter calcoaceticus Alcaligenesfaecabs Aktug and Karapinar 1986

Aeromonas hydrophila Brevibactenum linens Bayoumi 1992
Bacillus subtihs Envrnra caroiovora Beuchat 1994
Beneckea natnegens Flavobactenum suaveolens Deans and ktchie 1987
Brochothnr thermosphacta Laaobacrllus bulgancus El-Kady et a1 1993
Citrobacterfreundit Leuconostoc cremons
Table 2. continued
Inhibited Inhibited
Mint Clostridiumsporogenes Micrococcus lufeus
(cont) Enterobacter aerogenes Salmonella Typhimurium
Escherichia coli Staphylococcus aureus
Klebsiella pneumoniae Streptococcus thermophilus
Loctobacillusplantarum
Proteus vulgans
Salmonella F’ullorum
Serratia mnrcescens
Streptococcusfaecalis
Yersinia enrerocolifrca
Onion Escherichia coli None Abdou er al. 1972

Salmonella Typhimurium kuchat 1994
Shigella dysenteriae Hargreaves er al. 1975
Staphylococcus aureus Hughes and Lawson 1991
Huhtan.cn 1980
Shelef 1984
Oregano A erobacter aerogenes None kuchat 1994

Bacillus subrilis Ting and Deibel 1992
Clostridium botulinum Huhtanen 1980
Escherichia coli Ismaiel and Pierson 1990a. b
Lnctobacillus plantarum Kivanc and Akgul 1986
Leuconostoc mesenteroides Kivanc ef al. 1991
Listeria mnocytogenes Shelef 1984
Proteus vulgaris
Sraphylococcus aureus
Table 2 . continued

Inhibited Inhibited
Rosemary Acinetobacter calcoacetrcus A lcaligenes faecahs Beuchat 1994
Aerobacter aerogenes Brevibactenum linens Deans and Ritchie 1987
Aeromonas hydrophila Brochothnx thermosphacta El-Kady et al. 1993
Bacillus anthracis Erwinia carotovora Ting and Deibel 1992
Bacillus cereus Lactobacillusplantarum Farag et al. 1989b
Bacillvr megaterium Leuconostoc cremoris Farboad et al. 1976
Bacillus subtilis Micrococcus lureus Hargreaves et al. 1975
Beneckea natriegens Yersinia enterocolitica Huhtanen 1980
Citrobacterfreundii Kivanc and Akgul 1986
Clostridium botulinum Shelef 1984
Clostridium sporogenes Shelef et al. 1980
Flavobacterium suaveolens
Micrococcus (Sarcina)
Mycobacteriumphlei
Proteus vulgaris
Pseudomonasfluorescens
Pseudomonas pyocyanea
Salmonella Pullorum
Serratia marcescens
Serratia rhadnii
Staphylococcus epidermidis
Vibno parahaemolyticus
Sage A erobacter aerogenes A cinetobacter calcoaceticus Auouz and Bullerman 1982

Bacillus megmerium Aeromonas hydrophila Beuchat 1994
Bacillus subtilis Alcaligenesfaecalis Deans and Rtchie 1987
Beneckea natriegens Brevibacterium linens Ting and Deibel 1992
Clostridiumbotulinum Brochoihrix thermosphacta Farag et al. 1989b
Enterobacter aerogenes Citrobacterfreundii Hargreaves et al. 1975
Flavobanerium suaveolens Clostridium sporogenes Hefnawy er 01. 1993
Listeria monocytogenes Envinia carotovora Huhmen 1980
Mycobacteriumphlei Klebsiella pneumoniae Kivanc and Akgul 1986
Pseudomonasfluorescens Lactobacillusplantarum Shelef 1984
Staphylococcus aureus Leuconostoc cremoris Shelef et al. 1980
Staphylococcus epidemidis Micrococcus luteus
Salmonella hllonrm Yersinia enterocolrtica
Serratia marcescens
Streptococcus nasik
Vibrio parahaemolyticus
Table 2. continued
Inhibited Inhibited
Tarragon Aerobacter aerogenes Clostridiurn botulinurn Huhtanen 1980
Bacillus subtilis Kivanc and Akgul 1986
Escherichia coli
Proteus vulgaris
Thyme A cinetobacter calcoaceticus Clostridium sporogenes Aktug and Karapinar 1986
Aerobacter aerogenes Leuconostoc cremons Arras and Grella 1992
Aeromonas hydrophila Pseudomonas pyocyanea Azzouz and Bullerrnan 1982
AIcaligenes faecalis Beuchat 1994
Bacillus anthracis Deans and Ritchie 1987
Bacillus cereus El-Kady et al. 1993
Bacillus subtilis Farag et al. 1989b
Beneckea natriegens Huhtanen 1980
Brevibacterium linens Kivanc and Akgul 1986
Brochothrir ihemsphacta Shelef 1984
Citrobacterfreundii
Enterobacter aerogenes
Erwinia carotovora
Escherichia coli
Flavobacierium suaveolens
Lnctobacillus plantarum
Micrococcus (Sarcina)
Micrococcus luteus
Mycobactenurn phlei
Proieus vulgaris
Pseudomonas puorescens
Salmonella Pullorum
Serratia marcescens
Staphylococcus faecalis
Streptococcus faecalis
Streptococcus nasik
Vibrio parahaemolytrcus
' Adapted from Billing and Sherman 1988.
Effect of temperature on the antimicrobial properties of spices is dubious.

Extraction of essential oil of spices requires high temperature steam distillation.
Moyler (1994) reported that CO, extraction at low temperature and steam
distilled extraction at high temperature showed similar results. Oregano, sage

and cloves inhibited Curnpylobucfer jejuni after 16 h of simmering at 25C and
42C (Deibel and Banwart 1984).
ANTIMICROBIAL PROPERTIES OF SPICES
Spices have been found to have antimicrobial activities against bacteria,

fungi, and viruses. The use of spices in food systems might provide a hurdle
effect. The hurdle effect is defined as the contribution of several factors to
produce stable and safe products. Heating, chilling, freezing, freeze-drying,
curing, salting, sugar-addition, acidification, fermentation, smoking and oxygen
removal are some processes used in food processing. In general these parameters
or hurdles can be classified as high temperature, low temperature, water activity
(aw) level, pH, redox potential, preservative and competitive flora (Leistner
1992). Beuchat and Golden (1989) summarized spices and herbs used in foods
that possess antimicrobial activity (Table 3 ) .
TABLE 3.
SPICES AND HERBS USED IN FOOD WITH ANTIMICROBIAL ACTIVITY’
Achiote Cinnamon Mace Pepper
Allspice (pimento) Citronella Mandarin Peppermint
Almond (bitter) Clove Marjoram Rosemary
Angelica Coriander Musky bugle Sage
Basil (sweet) Dill Mustard Sassafras
Bay (laurel) Elecampane Nutmeg Spearmint
Bergamot Fennel Onion Star anise
Calrnus Garlic Orange Tarragon (estragon)
Cananga Ginger Oregano Thyme
Caraway Lemon Paprika Turmeric
Cardamom Licorice Parsley Verbena
Celery Lime Pennyroyal Wintergreen
* Adapted from Beuchat and Golden 1989

One of earliest studies on the antimicrobial activity of spices was reported

by Chamberland in 1887 in which cinnamon oil was found to be lethal to
anthrax spores (Davidson et al. 1983). Earlier studies on the antimicrobial
potential of cinnamon and cloves found that water infusion of cinnamon and
clove inhibited the growth of eight species of yeast, including Saccharomyces
cerevisiae (Shelef 1984; Zaika 1988; Conner 1993). Nakatani (1994) reported
that Dold and Knapp examined the antimicrobial activity of 27 spices against 8
microorganisms and found that garlic was the most inhibitory against all
microorganisms tested, followed by onion, nutmeg and clove. Bullerman (1974)
found that 1% ground cinnamon in raisin bread significantly reduced the growth
of Aspergillus parasiticus and aflatoxin production, and 2% ground cinnamon
was effective more than 95% in preventing the formation of aflatoxins B, and
G, in vitro.
Some of the biological activities of spices are antifeedant, insecticide,
vermicide, vermifuge, antihelminthic, antiviral, antifungal, antimicrobial and
antioxidant actions (Beckstrom-Sternberg and Duke 1994). The antimicrobial
properties of plant essential oils, their chemical constituents and mode of action
have been intensively investigated against food spoilage and poisoning bacteria,
spoilage and mycotoxic fungi, pathogenic yeasts, and animal and plant viruses
(Kivanc and Akgul 1986; Farag et al. 1989a, b; Deans and Ritchie 1987;
Cosentino et al. 1999; Lis-Balchin and Deans 1997; Deans and Svoda 1988,
1989; Cruz er al. 1989; Carson et al. 1995, 1996; Shelef 1984; Jay and Rivers
1984; Shapiro el al. 1994; Sivropoulou et af. 1997; others).
The most frequently used spices among different cuisines are onion, black
and white pepper, garlic, capsicums, lemon and lime juice, parsley, ginger,
coriander, cinnamon, cloves, thyme and others (Table 4) (Billing and Sherman
1998).
Plants contain a variety of compounds called "secondary" plant compounds
grouped as glucosides, saponins, tannins, alkaloids, essential oils, organic acids
and others (Fraenkel 1959). Phytoalexins, low molecular weight compounds
biosynthesized against a variety of stresses, have both antimicrobial and
antifungal properties (Beuchat 1994; Beuchat and Golden 1989). They are
produced after infection as a defense mechanism against microbial infection
(Naidu et al. 2000). These compounds interfere with the cell membrane
associated functions (Beuchat and Golden 1989). Plant pigments such as
anthocyanins inhibit the enzymatic mechanisms and cellular growth
(Somaatmadja er al. 1964). The major antimicrobial components of spices are
in their essential oils (Shibasaki 1982). Each compound in spices and herbs
exhibit different biological activity. Major compounds in some commonly used
spices in food are tabulated in Table 5 (Duke 1994).
TABLE 4.
PROPORTIONS OF SPICES USED IN MEATBASED RECIPES OF VARIOUS CUISINE’
Proportion of Spices
Recipes
~~ ~~
> 0.6 Onion, black pepper and white pepper
0.2-0.6 Garlic, capsicums, lemon, lime, and parsley

0.1-0.2 Ginger and bay-leaf
Less than 0.1 Coriander, cinnamon, cloves, thyme, green pepper, paprika, allspice, cumin,
nutmeg, turmeric, celery seed, cardamom, saffron, mustard, basil, lemon
grass, dill weed, oregano, galangal (laos), mint, tamarind, sesame, mace,
rosemary, sage, marjoram, anise seed, caraway, tarragon, juniper, capers,
horseradish, fennel, fenugreek and savory
’ Adapted from Billing and Sherman 1998.
A large volume of data of antimicrobial activity of spices is available, but

grouping of spices according to their antimicrobial activity is very difficult.
Zaika (1988) classified spices according to their antimicrobial activities (Table
6). Test medium (i.e., water content, liquid medium, solid medium, food or
beverage), spice and its active components (i.e., the method of experiment or
process, concentration, geographic origin, climate) and the microorganisms
tested (i.e., inoculum size, origin of culture, strain difference, spore forming
microorganisms) were the common factors that influence the antimicrobial
activity of spices and their extracts, essential oils or active components (Zaika
1988). Food systems due to their complex structures require higher amounts of
essential oils or their components than laboratory media (Shelef 1984; Shelef et
al. 1984; Zaika 1988). Protein and fat components of foods bind essential oil
compounds, reduce their availability, and protect microorganisms from their
antimicrobial action (Shelef 1984; Raccach 1984). Zaika (1988) summarized the
parameters of antimicrobial activity of spices as follows:
“(1) A variety of methods have been reported for testing the antimicrobial
activity of spices, herbs and their components.
(2) The degree of observed microbial inhibition depends on the method
employed to test for microbial activity.
(3) Microorganisms differ in their resistance to a given spice or herb.
(4) A given microorganism differs in its resistance to various spices and herbs.
(5) Bacteria are more resistant than fungi.
(6) The effect on spores may be different than that on vegetative cells.
(7) Gram-negative bacteria are more resistant than Gram-positive bacteria.

(8) Effect of spice or herb may be inhibitory or germicidal.
(9) Essential oils in contact with microorganisms in the test media possess
greater germicidal powers than they do in their vaporous state.
(10) Spices and herbs harbor microbial contaminants.
(1 1) Spices and herbs may serve as substrates for microbial growth and toxin
production.
(12) Amounts of spices and herbs added to foods are generally too low to
prevent spoilage by microorganisms.
(13) Active components at low concentrations may interact synergistically with
other factors (NaCI, acids, and preservatives) to increase preservative
effect.
(14) Decreased antimicrobial activity of spices and herbs in food may be due
to partitioning of active components into the lipid phase.
(15) Nutrients present in spices and herbs may stimulate growth and/or
biochemical activities of microorganisms.
(16) The extent to which spices inhibit microbial growth depends on their
source and processing. ”
ANTIBACTERIAL PROPERTIES OF SPICES
Use of spices with antioxidant, antimicrobial, flavor enhancer and

fermentation aid properties is very important to create new products (Williams
and Brown 1987). Carnasol and ursolic acid, two constituents of rosemary,
inhibited the growth of food spoilage bacteria. Carnasol possessed a higher
antimicrobial activity compared to BHT and BHA (Collins and Charles 1987),
and an antioxidant activity similar to BHT and superior to BHA (Wu el al.
1982). Addition of spices (onion powder, garlic powder, white pepper and
celery seed) increased the hedonic score of palatability of chicken broth (Chi and
Chen 1992).
Deans and Ritchie (1987) examined the antimicrobial properties of fifty
plant essential oils against 25 genera of bacteria. Each plant essential oil was
found to be inhibitory to at least one test bacterium. Thyme, cinnamon, bay,
clove, almond (bitter), lovage, pimento, marjoram, angelica and nutmeg
essential oils displaced the greatest inhibitory properties. Gram-positive and
Gram-negative bacteria were both affected by essential oils. Ueda et al. (1982)
examined the ethanolic extracts of spices and herbs for inhibiting of bacteria and
fungi at different pHs. Clove extract showed remarkable antibacterial activity
against all organisms tested and oregano and cinnamon exhibited wide inhibitory
spectrum. Gram-negative bacteria exhibited less sensitivity compared to Gram-
positive bacteria. Ouattara et al. (1997) examined the inhibitory properties of
TABLE 5.
SOME BIOLOGICALLY ACTIVE COMPOUNDS IN SPICES'
Rosemary Cinnamon Thyme Oregano Bay

Anethole Benzaldehyde Borneol Anethole Acetic acid
Apigenin Camphene- Bornyl acetate Apigenin Benza1dehyde
Ascorbic acid Camphor Caffeic acid Borneol Borneol
Borneol Caryophyllene Camphene Cadinene Bornyl acetate
Bornyl acetate 1.8-Cineole Delta-3-Carene Caffeic acid Cadinene
Caffeic acid Cinnamaldehyde Beta-Carotene Camphor Delta-3-Carene
Camphor Cuminaldehyde Carvacrol Delta-3-Carene Camphene
Delta-3-Carene p-Cymene Chlorogenic acid Beta-Carotene Caryophyllene
Carveol Eugenol 1&Cineole Carvacrol 1&Cineole
Caryophyllene Famesol p-Cymene Carvone Costulonide
Chlorogenic acid Furfmal Geraniaol Caryophyllene Cubebin
1,8-Cineole Guaiacol Limonene 1,SCineole p-Cymene
p-Cymene Limonene Linalool p-Cymene Eugenol
Genkwanin Linalool Methionine Geraniol Geraniol
Geraniol Methyl eugenol Myrcene Kaempferol Limonene
Glycolic acid Methyl salicylate Niacin Limonene Linalool
Limonene Myrcene Pinene Linalool Methyl eugenol
Linalool Niacin Rosmarinic acid Luteoline Myrcene
Methyl eugenol Pinene Terpinen4-ol Niacin Pinene
Niacin Piperitone Terpineol Pinene Terpinen-4-01
Pinene Safrole Thymol Rosmarinic aci Terpineol
Rosmarinic acid Terpmeol Tryptophan Terpinene
Safrole Ursolic acid Thymol
Terpinene Ursolic acid
Thujone
Ursolic acid
Garlic Cloves AlIspice Sage Vanilla

Ajoene Anethole Anethole Apigenin Acetaldehyde
Allicin Benzaldehyde Ascorbic acid Ascorbic acid Acetic acid
Alliin Carvone Cadinene Borneol Anisaldehyde
Allistatin-I Caryophyllene Delta-3-Carene Bornyl acetate Benzaldehyde
Allistatin-I1 Chavicol Beta-Carotene Camphor Benzoic acid
Arginine Cinnamaldehyde Caryophyllene Beta-Carotene Cresol
Ascorbic acid Ellagic acid Copaene Caryophyllene Eugenol
Choline Eugenol p-Cymene Chlorogenic acid Furfural
Citral Eugenyl acetate Eugenol 1,8-Cineole Guaiacol
Diallyl disulfide Furfural Linalool Limonene Vanillic acid
Diallyl sufide Gallic acid Methyl eugenol Linalool Vanillin
Geraniaol Kaempferol Myrcene Myrcene Vanillyl alcohol
Glutamic acid Linalool Pinene Niacin
Linalool Methyl eugenol Selinene Pinene
Niacin Terpinen-4-ol Rosmarinic acid
Trypthophan Terpinene Terpinen-4-01
Terpinene
Thujone
Ursolic acid
' Adapted from Duke 1994.

TABLE 6.
POTENT ANTIMICROBIAL ACTIVITY OF SPICES’
Antimicrobial activity Spice
Strong Cinnamon, clove, mustard
Medium Allspice, bay leaf, caraway, coriander, cumin, oregano, rosemary,

sage, thyme
Weak Black pepper, red pepper, ginger
Adapted from Zaika 1988
cinnamon, clove, cumin, garlic, oregano, black pepper, pimento and rosemary
essential oils against meat spoilage bacteria, Carnobacterium piscicola, L.
curvatus, L. sake, Brochothrix thermosphacta, P . jluorescens, and Serratia
liquefaciens. Clove, cinnamon, pimento, and rosemary essential oils exhibited
the most inhibitory activity. The inhibitory effects of clove and pimento were
attributed to the presence of eugenol and cinnamaldehyde in cinnamon oil.
Although the essential oils of other spices with low inhibitory activity contained
antimicrobial compounds such as eugenol, thymol, they were very small in
quantity to exhibit antimicrobial activity.
In general, Gram-positive bacteria are more sensitive than Gram-negative
bacteria and Pseudomonas species are least sensitive to bioactive agents. The
outer cell membrane of Gram-negative organisms has several lipid compounds
that protect the cells from the antimicrobial agents (Shelef ef al. 1980; Branen
et al. 1980; Farag et al. 1989b; Russell 1991). However, B. fhemzosphacta, a
Gram-positive bacterium, was as resistant as Gram-negative bacteria to the spice
oils (Ouattara et al. 1997). Gram-positive cocci (excluding sporulating Gram-
positive bacteria) are more sensitive than Gram-negative bacteria to many
biocides (Russell 1991).
MacNeil and Mast (1973) reported that 0.08% spice extracts in
mechanically deboned chicken frankfurters to substitute for nitrites and nitrates
increased the lag phase of microbial growth for an extended period of time when
stored at 45F (7.2C). Hall and Maurer (1986) tested effectiveness of spice
extracts of mace, bay leaf, nutmeg, white pepper, and black pepper against C.
botulinum in turkey frankfurter slurries as substitutes for nitrites. Extracts were
added into mechanically deboned turkey meat frankfurter formulation. Alcohol
extracts of mace (31 ppm), nutmeg, black pepper, white pepper and bay leaf
(125 ppm) inhibited C. botulinum toxin production in turkey frankfurters (Hall

and Maurer 1986). After an incubation period, supernatants of each formulation
with different spices were injected into mice to examine the effectiveness of
spice extracts on the growth of C. botufinum and toxin production, and results
were expressed as percent death (Table 7). Huhtanen (1980) reported that 31
ppm alcoholic extracts of mace and achiote (Cannato, Bixa orellanal) were the
most inhibitory spices among 33 spices tested against C. botulnium. Nutmeg,
bay leaf, white and black pepper (125 ppm) were moderately inhibitory while
paprika, rosemary, cloves, oregano, turmeric and thyme (500ppm) were slightly
inhibitory.
TABLE 7.
EFFECTIVENESS OF SPICE EXTRACTS ON CLOSIXIDIUM BOTULJNUM INHIBITION
IN TURKEY FRANKFURTER SLURRIES'
Spice Amount Trial PH Number of Mortality
@Pm) Deaths (%)
Mace 31 1 5.6 0120 0
2 5.8 0120 0
3 6.0 0120 0
Black pepper 125 1 5.7 0120 0

2 5.6 3/20 15
White pepper 125 1 5.6 0/20 0

2 5.8 4/20 20
Bay leaf 125 1 5.8 0120 0

2 5.9 0120 0
3 5.8 0120 0
Nutmeg 125 1 5.9 0120 0

2 6.0 0120 0
3 5.8 0120 0
I Adapted from Hall and Maurer 1986.
Shelf-life of chicken, beef and mutton cuts sprayed with water extracts of
ginger, garlic and onion were extended at ambient temperature. Garlic had
higher antimicrobial activity with longer shelf-life than ginger and onion
treatments (Ziauddin et al. 1996). Garlic juice (1:125,000) was found to inhibit
the growth of Staphylococcus, Streptococcus, V. cholerae. B. typhosus, B.
dysenteriae and B. ententidis, and also zoopathogenic fungi and many strains of
yeast (Block 1985). Addition of as little as 1% (v/v) garlic extract completely

inhibited the growth of E. coli, Salmonella Typhosa, S. dysenteriae and S.
aureus. Addition of 4 % (v/v) onion extract completely inhibited the growth of
S. dysenteriae and S. uureus and reduced the number of E. coli and S. Typhosa
by 48.3 and 95.3%, respectively, (Al-Delaimy and Ali 1970). E. coli was found
susceptible to garlic but more resistant to onion. The progeny of garlic and
onion treated S. Typhimurium showed the same susceptibility to garlic and onion
as the parental type, indicating that the progenies were not resistant mutants
(Johnson and Vaughn 1969).
Farbood et al. (1976) examined antibacterial effect of rosemary extract on
the growth of total bacterial count and the cultures of E. coli, E. aerogenes, P.
jluorescens, S. Typhimurium, and S. aureus in mechanically deboned poultry
meat, turkey breast, and beef. Rosemary extract (1% w/v) had a very little
bactericidal effect on E. coli, E. aerogenes and P. fluorescens. The population
of S. Typhimurium and S. aureus were reduced 43.2 and 99.9% in tryptic soy
broth after 24 h incubation at 37C with 1% (w/v) rosemary extract. However,
rosemary extract (1 % w/w) had no bactericidal effect on the growth of S. aureus
in mechanically deboned poultry meat incubated at 35C and 5C. Only 5%
rosemary extract showed bactericidal effect against S. aureus in mechanically
deboned poultry meat. When rosemary extract and the growth medium were
sterilized together, antibacterial effect of rosemary extract significantly increased
against S. Typhimurium and S. aureus. Mendoza-Yepes et al. (1997) evaluated
the inhibitory effects of a commercial mixture of 50% essential oils of rosemary,
sage, and citrics and 50%glycerol. Essential oil mixture inhibited Gram-positive
bacteria, L. monocytogenes, L. innocua, S. aureus, M . luteus and L. brevis at
40 ppm in culture media. However, higher concentrations of essential oils were
required to inhibit the growth of Gram-negative bacteria, Salmonella
Choleraesuis, E. coli 0157:H7, E. cloacae and P. aeruginosa, and no inhibitory
effect was determined against P. fluorescens. Aktug and Karapinar (1986)
examined the inhibitory effect of thyme, mint, bay leaves and their alcohol
extracts on the growth of S. Typhimurium, V. parahaemolyticus and S. aureus
in a medium. S. Typhimurium was found to be the least sensitive to these
spices. Thyme was the most inhibitory against the bacteria tested. Farag et al.
(1989b) evaluated the antimicrobial effect of the essential oils of sage, rosemary,
cumin, caraway, clove, and thyme against P. fluorescens, S. marcescens, E.
coli, Surcina spp., Micrococcus spp., S. aureus, B. subtilis. Mycobacterium
phlei, and S. cerevisiae. Clove and thyme essential oils (0.75 to 1.5 mg/mL) and
their active compounds were highly inhibitory against the cultures tested while
others exhibited moderate or no antimicrobial activity. Acid fast M . phlei was
more sensitive to the essential oils tested than Gram-positive and Gram-negative
organisms. Nadal et al. (1973) showed that the essential oil of bay leaf, pimento
berry, pimento leaf and cloves having eugenol as a major component exhibited
22 E. CEYLAN and D.Y.C.FUNG
the minimum inhibitory concentration from 10 to 100 pg against Gram-positive,

Gram-negative, and yeast and fungi.
Hao et al. (1998a) evaluated antibacterial activity of alcohol extracts (0.1
mL) of angelica root, banana puree, bay, caraway seed, carrot root, clove
(eugenol), marjoram, pimento leaf, and thyme against Aeromonas hydrophila
and L. monocytogenes on skinless chicken breast meat. Eugenol and pimento
extract inhibited the growth of both bacteria. Eugenol treated chicken breast
meat stored at 5C for 14 days had 4 log cfu/g less growth of A . hydrophila
compared to control sample. Stecchini et al. (1993) reported that clove extract
inhibited the growth of A . hydrophila in cooked pork. Cinnamon and clove
exhibited greater inhibition on the growth of L. monocytogenes compared to
garlic, onion, and mustard (Bahk et al. 1990). Allspice (pimento) and sage
exhibited antilisterial effect in tryptose broth (Hefnawy et al. 1993) but the
antilisterial effect of spices in foods was less than the laboratory medium.
Skinless chicken breast samples with eugenol and pimento extracts had 1-2 log
cfu/g less L. monocytogenes than control samples during 14 days of storage at
5C. Eugenol and pimento extracts exhibited very potent inhibition against A .
hydrophila and L. rnonocytogenes at a low initial inoculation level (1 log cfu/g)
and the lag phase of both bacteria was extended. Eugenol and pimento extract
were found to be bactericidal against A . hydrophila and L. monocytogenes on
cooked beef (Ha0 et al. 1998b). However, a stronger antibacterial effect was
observed with chicken samples. This effect might be attributed to the absorption
of essential oils in the high lipid content of beef samples (Ha0 et al. 1998a).
Solubilization of essential oils in lipid fraction of foods reduces their
antimicrobial activity (Ismaiel and Pierson 1990a; Shelef et al. 1984). In a study
of antilisterial effect of 18 spices in laboratory medium and meat system,
rosemary ( 2 0.5% w/v) and cloves (1 1.0% w/v) were antilisterial to L.
monocytogenes Scott A in laboratory medium (Pandit and Shelef 1994).
Rosemary oil at a concentration of 10 pL/lOO mL exhibited bactericidal effect
against L. monocytogenes in broth. Among four major components of rosemary
oil (cineole, bornole, a-pinene, and camphor), a-pinene at 1 pL/lOO mL
produced listeriostatic effect in laboratory medium and rosemary oleoresins had
no antilisterial effect up to 100 mg/lOO mL concentration. Addition of 0.5%
(w/w) ground rosemary and 1% (v/w) rosemary oil delayed the growth of L.
monocytogenes in pork liver sausage emulsion stored at 5C for 50 days. Higher
concentration of ground rosemary and rosemary oil was needed to obtain
antilisterial effect in food samples. A basil essential oil component, methyl
chavicol, was bactericidal to Aeromonas hydrophila and P. jluorescens (Wan et
al. 1998). Parsley (0.12 - 8.0%)was found to have antimicrobial furocoumarins
that inhibited the growth of L. monocytogenes, E. coli 0157:H7 and spoilage
microorganisms (Manderfeld ef al. 1997). Four varieties of fresh and freeze-
dried parsley leaves had different amounts of furocoumarins. Photoactive
furocoumarins isolated from all varieties of parsley inhibited the growth of E.

coli Bs-1, E. coli 0157:H7, Erwinia carorovora, L. monocytogenes, and L.
innocua by the bioassay method. However, Pseudomonasfragi was not inhibited
by furocoumarins. Ting and Deibel (1992) evaluated antilisterial effect of 13
spices against three different strains of L. monocyrogenes on TSA agar. Clove
(0.6 to 0.7% w/v) and oregano (0.5 to 0.7% w/v) were the most inhibitory
against these three cultures followed by sage (0.6 to 0.7% w/v), rosemary (0.6
to 0.7% w/v) and nutmeg (0.6 to 0.7% w/v). Cloves, oregano and sage
suppressed the growth of L. monocytogenes Scott A by 2 log cfu/mL in TSB
broth incubated at 4C for 4 days and 24C for 24 h. Antilisterial effect of sage
enhanced at 4C, however, oregano and cloves (1% w/w) in beef slurry at 4 and
24C did not exhibit antilisterial effect. Black pepper, garlic, cinnamon, red
pepper, chili, paprika, parsley and mustard (3% w/v) had no antilisterial effect
on the growth of L. monocytogenes strains tested. The presence of high amount
of protein and fat require higher amount of spices or their essential oils (Shelef
er al. 1984), and fat content might prevent penetration of these substances into
the cells forming a coating layer on the surface of the cells (Farbood et al.
1976). Among 93 commercial essential oils tested against 20 L. monocytogenes
strains, white camphor, lemon verbena, angelica root, cassia, cinnamon leaf,
clove leaf, clove bud, basil, bergamot, pimento, bay, eucalyptus radiata and
citriodora, tea-tree and lemongrass exhibited antilisterial activity against all
Listen'a strains tested. Essential oils containing monoterpenes, eugenol,
cinnamaldehyde, thymol, and also citronellol, limonene and geraniol had strong
antilisterial activity tested. The same essential oil had variable antilisterial
activity against different strains and different essential oil samples of the same
spice had different antilisterial activity (Lis-Balchin and Deans 1997).
Deibel and Banwart (1984) tested the antimicrobial effect of oregano, sage
and ground cloves (0.1, 0.5 and 1.0%), commonly used spices in red meat and
poultry preparations, against the growth of C. jejuni in a liquid medium at 4C,
25C and 42C. A great reduction of C. jejuni was observed at 42C with 0.5 and
1.O% of each spice but cell growth was recorded after 16 h of incubation. More
than a 3.0 log cfu/mL was determined in the presence of sage and oregano at
25C and less than a 1.0 log cfu/mL was determined in the presence of the tree
spices at 4C after 48 h incubation. Smith-Palmer er al. (1998) evaluated
antimicrobial properties of spice essential oils against C. jejuni, S. Enteritidis,
E. coli, S. aureus and L. monocytogenes (Table 8 ) . The essential oils of bay,
cinnamon, clove and thyme were the most inhibitory among spice oils tested and
bacteriostatic at a concentration of 0.075%.L. monocytogenes was very sensitive
to nutmeg. At 35C, 0.01% of the oil of nutmeg was bacteriostatic and 0.05%
was bactericidal, however, at 4C, 0.5% of the oil of nutmeg was bacteriostatic
and 0.1 % was bactericidal. Shelef et al. (1980) tested 24 Gram-positive and 22
Gram-negative foodbome bacteria to sage, rosemary and allspice treatments.
TABLE 8 .
BACTERIOSTATIC CONCENTRATION (96) OF SPICE ESSENTIAL OILS’
Essential oil C. jejuni S. enteritidis L. rnonocytogenes E. coli S. aureus-

Aniseed >1 >1 >1 >I >I
Basil 0.25 0.1 0.05 0.25 0.1
Bay 0.075 0.05 0.02 0.05 0.05
Clove 0.05 0.04 0.03 0.04 0.04
Cinnamon 0.05 0.05 0.03 0.05 0.04
Fennel >1 >1 >1 >l >1
Garlic >I >1 >1 11 >1
Ginger >1 >1 >1 >1 11
Marjoram 0.25 >1 0.02 >1 0.05
Nutmeg >1 >1 <0.01 >1 >1
Onion >1 >1 <1 >1 >I
Peppemint 0.1 >1 0.03 >1 0.04
Rosemary 0.5 >1 0.02 >1 0.04
Sage >1 >I 0.02 >1 0.075
Spearmint 0.25 0.25 0.04 0.25 0.075
Thvme 0.04 0.04 0.02 0.05 -_0.02

’ Adapted from Smith-Palmer et at. 1998.
Salmonella Typhimurium required 10 times more amount of sage for inhibition

of in broth than B. cereus. The antimicrobial activity of sage increased with
increase in salt and water content but decreased with increase in fat and protein
content. The antimicrobial activity of sage increased with increase in salt and
water content but decreased with increase in fat and protein content. Shelef et
al. (1984) evaluated inhibitory effect of sage on the growth of S. aureus, B.
cereus, Pseudomonas spp. and S. Typhimurium in laboratory medium, chicken-
noodle, boiled rice and strained beef. Inhibitory effect of sage in chicken-noodle
( > 1%) decreased compared to laboratory medium (0.1 to 1%). In nutrient

broth, 0.1, 0.4, 0.5 and 1.0% of sage inhibited the growth of B. cereus, S.
aureus, Pseudomonas spp. and S. Typhimurium, respectively. In strained beef
little or no inhibition was observed at 2.5 % . B. cereus spores exhibited a similar
pattern as vegetative cells against sage. The authors concluded that the
antimicrobial effect of sage decreased in food systems compared to laboratory
medium and with fat and protein content, and increased with water content.
Karapinar and Aktug (1987) found that eugenol ( 2 100 pg/mL) was the most
inhibitory essential oil component against S. Typhimurium, S. aureus and V.
parahuemolyticus followed by thymol, anethole and menthol.
The essential oil of sage (Salviafrucficosa)and its components, 1&cineole
(47.48%), a-thujone (4.32%), /3-thujone (7.61 %), and camphor (9.04%),
exhibited antimicrobial activity against E. coli, P. aeruginosa, S.Typhimurium,
Rhizobium leguminosarum and B. subtilis cultures. S. Typhimurium was the
most resistant and P. aeruginosa was the most sensitive to the essential oil
components of sage. The three main components showed a certain degree of
antimicrobial activity against the bacterial cultures tested but 1,8-cineole, a- and
p-thujone possessed higher antimicrobial activity than camphor (9.04 %)
(Sivropoulou et ul. 1997).
Dickens et al. (2000)evaluated effectiveness of a commercial herbal extract
on a NaCl carrier, Protecta I1 on the microbiological quality of broiler carcasses
during a stimulated chill at 1C for 45 min. Rinse diluents of control samples, tap
water and 2 % Protecta I1 solutions were analyzed for total aerobic counts,
coliforms, generic E. coli, and Campylobacter. Control samples had 3.7, 2.5,
2.1, and 2.0 log cfu/mL for total aerobic counts, coliforms, generic E. coli, and
Campylobacfer, respectively. Water treatment alone significantly reduced the
bacterial loads to 2.6, 1.4, 0.7, and 0.9 cfu/mL for total aerobic counts,
coliforms, generic E. coli, and Campylobacter, respectively. The 2 % solution
of herbal extract, Protecta 11, treatment caused further reductions of microbial
populations of broiler carcasses to 0.06, 0.04, 0.01, and 0 cfu/mL for total
aerobic counts, coliforms, generic E. coli, and Campylobacrer,respectively. No
visual or physical change to skin of broiler carcasses was observed. MacNeil et
al. (1973) reported that mechanically deboned poultry meat (85 % turkey meat
and 15% turkey skin) with 0.01 and 0.05% rosemary extract had lower total
plate counts for the first week of storage at 3C and lower TBA values as well.
Similarly, Cutter (2000) demonstrated the surface spray treatment of 2.5 %
commercial herb extracts dispersed in sodium citrate (Protecta I, pH 6.19) or
sodium chloride (Protecta 11, pH 5.06) against E. coli 0157:H7, S.
Typhimurium and L. monocytogenes on beef surfaces. After 7 days of storage
at 4C, the extract dispersed in sodium citrate reduced L. monocyfogenes 1.8 log
CFU/cm2, and the extract dispersed in sodium chloride reduced E. coli 0157:H7
and L. monocytogenes 1.9 and > 1.3 log CFU/cm*, respectively.
AN”GAL PROPERTIES OF SPICES
Fungi are not considered as the primary spoilage agents in meat unless
antibiotics are not employed. The genera Candida and Rhodurorula are the most
frequently found yeast in poultry. The genera Alternaria, Aspergillus,
Cladosporium, Geotrichum, Mucor. Penicillium and Rhizopus are isolated from
poultry (Jay 1996). Ismail et al. (2001) determined the profiles of yeast species
on 15 commercial raw, marinated, smoked, OK roasted chicken and turkey
products. Among the yeast isolates of 152 strains of 12 species, Yarrowia
lipolytica and Candida zeylanoides were 39 and 26% of the total isolates,
respectively. Ismail ef aZ. (2001) evaluated effectiveness of herb decoctions
against Y. lipolytica and natural aerobic microflora on raw chicken. The
population of Y. Zipolytica was significantly reduced in 100% decoctions of basil,
marjoram, sage, and thyme at 5C for 24 h. Decoction of 100% sage or thyme
significantly reduced the population of Y. lipolytica on chicken wings during
storage at 5C for 9 days but the growth of the yeast occurred during longer
storage. Hili ef al. (1997) reported that 51 essential oils tested against bacterial
cultures, P. aeruginosa, E . coli, S . aureus, and yeast cultures, C. albicans, S.
cerevisiae, Torulopsis utilis, and Schizosaccharomyces pombe showed
antimicrobial activity by inhibiting the growth of at least one microorganism.
Clove, coriander, cinnamon, cardamom, thyme, tea tree, marjoram, ho leaf,
rosemary, peppermint, palmarosa, lemon grass and sage essential oils possessed
stronger antimicrobial activity toward yeast species than the bacterial cultures.
P. aeruginosa was the most resistant organism and cinnamon had the most
potent antimicrobial activity (10-150 pglmL) (Hili et al. 1997).
Hydroxycinnamic acids, p-coumaric acid and ferulic acid, increased the lag
phase of S. cerevisiae at 100 and 50 ppm, and ferulic acid inhibited the growth
at 250 ppm (Baranowski et al. 1980). Vanillin (4-hydroxy-3-
methoxybenzaldehyde)has antimycotic activity and a structure similar to eugenol
(Beuchat and Golden 1989). Vanillin (2000 ppm), a major constituent of vanilla
beans, exhibited a significant inhibitory effect against the growth of food
spoilage yeasts, S. cerevisiae, Zygosaccharomyces rouxii, Debaryomyces
hansenii and 2. bailii in laboratory medium and apple puree at 27C for 40 days
storage (Cerutti and Alzamora 1996). Comer and Beuchat (1984a) evaluated the
sensitivity of heat-stressed yeasts, Candida lipolytica, Debaryomyces hansenii,
Hansenula anomala, Kloeckera apiculata, Lodderomyces elongisporus,
Rhodotorula rubra, Saccharomyces cerevisiae, and Torulopsis glabrata, to
essential oils of allspice, cinnamon, clove, garlic, onion, oregano, savory, and
thyme. Garlic oil interfered with the growth of all unheated yeast cultures tested
while the other essential oils with the exception of onion oil for S . cerevisiae and
oregano oil for R. rubra, had no effect on the growth of unheated yeast cultures.
Garlic oil had lethal effect on all heat stressed cells. Sublethally heat injured
yeast cultures showed different sensitivity to different essential oils. A slight

increase of sensitivity to essential oils was observed for K. apiculata while L.
elongisporus had an increased sensitivity to all essential oils tested. Heat
treatment and essential oil also caused changes in morphology, size, and pigment
production of cells. Eugenol at 625 and 293 pg/mL inhibited the growth of
medically important C. albicans (31 strains) and Cryptococcus neofomns (33
strains), respectively, (Boonchird and Flegel 1982). Vanillin at 1250 and 738
pg/mL inhibited the growth of C. albicans (31 strains) and Cryptococcus
neofomns (33 strains), respectively.
Moore and Atkins (1977)reported that an aqueous extract of garlic inhibited
the growth of fungi cultures from the genera Candida, Cryptococc~s,
Rhodotorula Torulopsis, and Trichosporon. Aqueous extract of garlic bulbs
inhibited the growth of most of over 60 economically and medically important
species of fungi tested (Tansey and Appleton 1975). Aqueous extract of garlic
was antifungal against 39 of 41 clinical isolates of C. albicans. Antifungal
activity gradually decreased at higher temperatures (i.e., 37C or higher)
proportionally with duration time. Activity was stable in acidic conditions and
destroyed in the presence of thiols such as L-cysteine or glutathione (Barone and
Tansey 1977).
The addition of ground oregano, thyme and their extracts into the growth
medium reduced the production of aflatoxins of Aspergillus parasiticus
(Salmeron et al. 1990). The volatile oil of Origanum syriacum (also called
Majorana syriaca) that contain carvacrol and thymol as the major components,
completely inhibited the mycelial growth of A . niger, Penicillium spp., and F.
oxysporum at a concentration of 0.1 pLlmL in yeast extract sucrose broth
(Daouk et al. 1995).
Akgul and Kivanc (1988) observed that among 10 spices tested only
oregano showed antifungal effect toward 9 fungi tested. Thymol and carvacrol
at 0.0025 and 0.05% (w/v), and pH 5.5 completely inhibited the growth of A .
flavus, A . niger, Geotricum candidum, Mucor spp., P. roqueforti and
Penicillium spp. in PDA agar. Black cumin seeds, coriander, cumin, dill, laurel
bay leaves, parsley, spearmint, sweet basil and white mustard had no inhibitory
effects against the fungal cultures tested. Among 29 spices tested, cloves, star
anise seeds and allspice inhibited the toxin production by Aspergillus spp.
Eugenol from clove and thymol from thyme ( < 4 mg/mL) completely inhibited
the growth of A . flavus and A . versicolor (Hitokoto ef al. 1980). Thymol at 500
pg/mL completely inhibited the growth of A . parasiticus (Buchanan and
Shepherd 1981). Cinnamon at 0.02, 0.2, 2.0, and 20% inhibited the growth of
A . parasiticus by 16,23, 3 1, and 100% and aflatoxin production by 25, 68, 97,
and loo%,respectively, (Bullerman 1974). Morozumi (1978) reported that o-
methoxycinnamaldehyde (OMCA) isolated from powdered cinnamon completely
inhibited the growth of A . parasitucus and A . flavus at 100 p g / m L and A .
ochraceus and A . versicolor at 200 pg/mL. It inhibited by over 90% of the

production of aflatoxin B, at 6.25 pg/mL, ochratoxin A at 25 pg/mL and
sterigmatocystin at 50 pg/mL.
ANTIMICROBIAL PROPERTIES OF ESSENTIAL

OIL COMPONENTS
Antimicrobial activity of the oils depends on the major constituents and their
concentration. The inhibitory effects of essential oils are mainly due to the major
component (Farag er al. 1989a). The small amounts of minor components might
also contribute the antimicrobial activity of the oils (Ouattara er al. 1997).
Essential oils are volatile compounds produced by plants as secondary
metabolites in particular cells or formed as glandular hairs (Hili er al. 1997).
Major component isolates from spices are shown in Table 9. Antimicrobial
properties of essential oils depend on genus, species, and geographical area
(climatic factors) of spices. For example, Origanum vulgare ssp. vulgare L. has
a very low essential oil constituent and its main compounds are sabinene, (Z)-p-
ocimene, /3-caryophyllene, and germacrene D, thymol and carvacrol. However,
Onganum vulgare ssp. hirtum has high essential oil constituents and its main
compounds are phenols, p-cymene, and y-terpinene (Russo er al. 1998).
Dorman and Deans (2000) examined the antimicrobial activity of the
volatile oils of black pepper, clove, geranium, nutmeg, oregano and thyme
against 25 different genera of bacteria including animal and plant pathogens,
food poisoning and spoilage bacteria. All the bacterial strains tested showed
some degree of sensitivity to volatile oils. The oil with the widest spectrum of
antibacterial activity was found to be from thyme, followed by oils from
oregano, clove, nutmeg, black pepper and geranium. The widest antibacterial
spectrum of an individual component was found to be thymol followed by
carvacrol, a-terpineol, terpinen-4-01, eugenol, ( k)-linalool, (-)-thujone, 6-3-
carene, cis-hex-3-an-1-01, geranyl acetate, (cis + trans) citral, nerol, geraniol,
menthone, 0-pinene, R( +)-limonene, a-pinene, a-terpinene, borneol, ( +)-
sabinene, y-terpinene, citronellal - terpinolene, 1,8-cineole, bornyl acetate,
carvacrol methyl ether, myrcene, /3-caryophyllene,a-bisabolol, a-phellandrene,
a-humulene, 0-ocimene, aromadendrene and p-cymene. Chemical structures of
major components of spices are shown in Fig. 1.
Phenolic compounds possess the highest antimicrobial properties followed
by alcohols, aldehydes, ketones, ethers and hydrocarbons (Kurita and Koike
1983). Most of the compounds isolated from sage are phenolic compounds
(Cuvelier er al. 1996). Wang er al. (1998) isolated ten phenolic compounds from
a butanol fraction of sage extract. The essential oils of spices are composed of
a complex composition of compounds. Bioactive ingredients in spices such as
sulfides, thiols, terpenes and their derivatives, phenols, glycosides, alcohols,

aldehydes, and esters have been investigated for their properties. Although some
phytochemicals have been identified, there are still many questions to answer
(Uhl 2000).
The majority of the antimicrobial components of spices are phenol
compounds with a hydroxyl group (-OH) (Beuchat and Golden 1989). Presence
of -OH group was found to be responsible for antimicrobial and antiaflatoxigenic
properties of thymol (Buchanan and Shepherd 1981). Basilico and Basilico
(1999) reported that at 1000 ppm essential oils of oregano and mint inhibited the
growth of A . ochraceus and ochratoxin A production in YES broth up to 21
days. The essential oil of thyme (Thymus serpylloides ssp. gadorensis) showed
a strong antibacterial effect against both Gram-positive and Gram-negative
bacteria. Phenolic compounds isolated from thyme were the most effective
against all bacteria tested followed by alcohols and hydrocarbons (Crespo et al.
1990). Steam distilled essential oil of French tarragon (estragon) yielded a
mixture of almost fifty compounds. The most inhibitory compounds in the oils
against a total of 10 Gram-positive and Gram-negative bacteria were
anisaldehyde, p-cymene, eugenol, limonene, linalool, menthol, cis-ocimene, a-
phellendrene, a-pinene and 0-pinene (Deans and Svoboda 1988).
The phenolic compounds such as carvacrol, eugenol and thymol are very
active antimicrobial agents (Nadal et al. 1973; Mahmoud 1994; Kim et al.
1995a; Sivropoulou et al. 1996; Suresh et al. 1992). The antimicrobial property
of oregano and thyme has been attributed to the essential oils terpenes carvacrol
and thymol (Beuchat 1976). Kim et al. (1995a) evaluated the antimicrobial
activity of citral, carvacrol, geraniol, a-terpineol, perillaldehyde, eugenol,
linalool, 0-ionone, limonene, nerolidol and citronellal against five foodborne
pathogens, E. coli, E. coli 0157:H7, S. Typhimurium, L. monocytogenes and
V. vulnificus. Carvacrol was the most inhibitory, and citral and geraniol had
potent antibacterial effect against the five bacterial pathogens tested.
Antimicrobial activity of the components was different for each bacterial culture
and the response of these cultures varied toward each component. In general,
bacteria are more resistant than fungi (Morozumi 1978; Zaika 1988), and Gram-
negative bacteria are more resistant than Gram-positive bacteria (Farag et al.
1989b; Zaika 1988).
Antibacterial activity of thymol and carvacrol varied among bacterial
species as well as in different strains of the same bacterial species. Three
different origanum essential oils had different amounts of two major
antimicrobial components carvacrol (0.43 to 75.98%) and thymol (0.44 to
31.8%). Of the 8 bacterial species tested, P. aencginosa was the most resistant
and Rhizobium leguminosancm was the most sensitive to these compounds.
While carvacrol and thymol possessed a strong antibacterial activity against
TABLE 9.
MAIN CONSTITUENTS AND BOTANICAL NAME OF SPICES
Name Botanical name Main constituents of

essential oiVoleoresin
Allspice Pimenta dioica Eugenol
Anise seed Pimpinella anisum Anethole
Star anise Illicium verum Anethole
Basil Ocimum basilicum d-linalool, methyl chavicol
Bay leaves Laurus nobilis Cineole
Caraway seed Carum carvi a-carvone
Cardamom seed Elettaria cardamomum Cineole, a-terpinyl acetate
Celery seed Apium graveolens d-limonene, sedanolide
Chervil Anthriscus cerefolium Methyl chavicol osmorhizol
Chives Allium schoenoprasum Diallyl sulfide
Cinnamon Cinnamomum zeylanicum Cinnamaldehyde
Cassia Cinnamomum cassia Cinnamaldehyde
Cloves SyzVgium aromaticum Eugenol
Coriander leaves Coriandrum sativum trans-2-decenal
Coriander seed Coriandrum sativum d-linalool
Cumin seed Cuminum cyminum Cuminaldehyde, y-terpinene
Dill seed Anethum graveolens d-carvone
(European and American)
Anethum sowa (Indian)
Fennel seed Foeniculum vulgare anethole
Fenugreek seed Trigonellafoenumgraecum anethole
Garlic Allium sativum dial1ylthiosulfinate
Ginger Zingiber oficinale Zingiberene, cineole, bomeol,
geraniol, zingerone
Mace Myristica fiagrans Myristicin, a-pinene, safrole
Marjoram Majorana hortensis Linalool, methyl chavicol, 4-
terpineol
Mint Mentha piperifa (peppermint) a-pinene, P-pinene, limonene,
Mentha spicata (spearmint) cineole (peppermint);
1-cawone (spearmint)
Mustard seed Brassica alba (yellow) Ally1 isothiocyanate
Brassica juncea (brown)
Brassica nigra (black)
Nutmeg Myristica fiagrans Myristicin, sabinene
Onion Allium cepa trans-91-propenyl cysteine
sulfoxide
Oregano Origanum vulgare Thymol, carvacrol
Paprika Capsicum annuum Carotenoids
Parsley Petroselinum crispum Little essential oil
Black pepper Piper nigrum Monoterpene hydrocarbons,
piperine
TABLE 9. continued
Chili pepper Capsicumfnrtescens Little to no essential oil,
capsaicinoids, carotenoids
Green pepper Piper nigrum Monoterpene hydrocarbons,
piperine
Pink pepper Schinus terebinthifolius a-pinene, limonene
Red pepper Capsicumfnrtescens Little to no essential oil,
Sweet pepper Capsicum annuum Little to no essential oil,
White pepper Piper nigrum Monoterpene hydrocarbons,
piperine
Poppy seed Papaver somniferum No essential oil
Rosemary Rosmarinus officinalis Borneol, a-pinene,
camphene, cineole,
rosmarinic acid
Saffion Crocus sativus 2,2,6-trimethyl-4,6-
cyclohexadienal, crocin,
picrocrocin
Sage Salvia officinalis a - and 0-thujones, borneol,
cineole
Savory Satureja hortensis Carvacrol, monoterpene
hydrocarbons
Sesame seed Sesamum indicum No essential oil
Tarragon Artemisia dracunculus Methyl chavicol, anethole,
y-terpinene
Thymus vulgaris Thymol
Turmeric Curcuma Ioiga Turmerone
bacteria tested, their biosynthetic precursor compounds y-terpinene and p-

cymene did not exhibit any antibacterial activity. Thymol was more effective
against Gram-negative bacteria than carvacrol (Sivropoulou et al. 1996). P.
aeruginosa has been found very resistant to many antibacterial agents but was
found to be sensitive to puleogone, isopulegol and piperitone (Sivropoulou et al.
1995).
OCH3
camphene
H2C=CHCH2N=C=
ally1 isothicyanate CH= CHCH3
anethole
CHzCHzCH2
I
CH,
3CACH2 chavicol
carvone cineole
/
CHO
cinnamaldehyde cinnamic acid
citral
CH3
I OH
pJyo
\ /
CHCH3
I
b"""'
CH2CH=CH2
coumarin CH3
eugenol
p-c ymene
COOH
CH~CH~COCHZCHOH(CH~)~CH~
CHO
+ @
OH OC2H5 OH
OCH3
HO
HO
gallic acid
HO
ferulic acid 6-ginger01

3C .H
OZH
H3C 3 'CH2
limonene
H~-C=CH-CH~-CH~-CC-CH=CH
CH3
I OH
I
linalool
I
CH3
'rCH3
CH3
menthol
CH3
CH3 I
I
63
alpha-pinen CHCH3
I
CH3
alpha-terpinen
beta-myrcene
If.
CH3
I CHO
CHCH3
I
CH3 H3 CH3
OH
@ OH
OCH3
thujone thymol vanillin
FIG. 1. CHEMICAL STRUCTURES OF MAJOR COMPONENTS OF SPICES

Carvacrol at 250 pL/mL, citral and geraniol at 500 pL/mL completely

inhibited the growth of S. Typhimurium and rifampicin-resistant (Rip) S.
Typhimurium in laboratory medium (Kim ef al. 1995b). However, higher
amounts of carvacrol, citral and geraniol (1.5%) was needed to kill S.
Typhimurium strains on fish cube samples due to the interaction of these
components with fish proteins and lipids.
Benjilali ef al. (1984) tested the antifungal activities of essential oils of three
chemotypes of mugwort, thyme, rosemary and eucalyptus against 13 strains of
Penicillium, nine of Aspergillus and 17 others. Overall, thyme was the most
effective followed by mugwort, rosemary and eucalyptus. Phenol containing
essential oils were more effective than ketone containing essential oils. Each
essential oil differed in its antifungal activity against different fungi and strains
of the same fungus. The fungi cultures tested exhibited a different degree of
sensitivity to different essential oils (Benjilali ef al. 1984).
Belaiche ef al. (1995) showed that eugenol possessed a significant
antimicrobial activity on S. aureus and closely followed linalool, while 1,8-
cineole had no significant activity. Carson and Riley (1995) stated that terpinen-
4-01 from tea tree essential oil possessed very high antimicrobial activity while
p-cymene had no antimicrobial activity.
Sarkar and Phan (1979) defined several naturally occurring phenolic
compounds in carrots. The number of L. monocyfogenes reduced upon contact
with whole and shredded raw carrots while the antilisterial effect was not
determined in cooked carrots. Shredded raw carrots possessed stronger
antilisterial effect than did whole raw carrots (Beuchat and Brackett 1990).
Volatile sulfur compounds might occur naturally in the food or are produced
as a metabolic product as result of environmental effects such as processing and
interruption of cell structure. Volatile sulfur compounds in food and their
chemistry were reviewed by Shankaranarayana ef al. (1974) and Block (1985).
Acrolein in onion and crotonaldehyde in garlic were reported to be the
antimicrobial fraction in onion and garlic. Various organic sulfur compounds
related to the flavor of garlic and onion are also believed to be antimicrobial
(Marth 1966; Barone and Tansey 1977; Sharma et al. 1979).
Flavor compounds of the genus Allium (garlic, onion, leek, and caucas)
have various biologically active sulfur compounds (Mochizuki and Yamamoto
1998). Characteristic volatile flavor compounds from intact garlic cloves are
enzymatically produced when the garlic tissues are ruptured. The volatile fresh
garlic flavor alk(en)yl thiosulfinates are enzymatically released by alliinase from
the precursor compounds of S-alk(en)yl-L-cysteine sulfoxides (Fig. 2; Schulz ef
ul. 1998). Thermally unstable thiosulfinate compounds are converted to alk(en)yl
polysulfides, dithiins, or ajoenes (Block 1985). Mochizuki and Yamamoto (1998)
also found trace amount of ally1 propyl sulfide, dipropyl trisulfide, and methyl
propyl trisulfide in garlic. Glutathione and y-glutamyl peptides were found as
the intermediate compounds to flavor precursors in Allium spp. (Lancaster and

Shaw 1989). Freeman and Whenham (1975) classified Allium species into three
groups: high proportions of propyl/propenyl cysteinsulfoxide (e.g .,onions), high
proportions of ally1 cysteinsulfoxide (e.g., garlic), and high methyl
cysteinsulfoxide (e.g., ornamental Allium species). An intact garlic bulb does not
contain the principal antimicrobial compound allicin, a diallyl thiosulfinate (2-
propenyl-2-propenethiol sulfinate). When tissue is disrupted, the precursor
compound alliin (S-allyl-L-cysteine-S-oxide) is hydrolyzed by allinase enzyme
that produces allicin and, pyruvate and ammonia.
RS(O)CH2CH(NH2)COOH
S-alk(en)nylcysteinesulfoxides (alliin)
1
RSOH + NH3 +
allinase
CH3C(O)COOH
i
RSSOR
Thiosulfinates
RSSR +
2RSSOR / RSS02R
Thiosulfinates
\ RSR + RSSR + SO2
Dialk(en)yl sulfides and disulfides
2 RSSR P RSSSR + RSR etc.

Dialk(en)yl disulfides Dialk(en)yl trisulfides
FIG. 2. FORMATION OF ALK(EN)YL SULFUR COMPONENTS IN ALLlUM PLANTS

(Adopted from Schultz er al. 1998)
MODE OF ACTION AND INHIBITORY MECHANISMS OF SPICES
Microbial species/strain, stressed microorganisms, type and amount of

antimicrobial compounds, number of microorganism present in food, presence
of other antioxidant compounds, presence of other antimicrobial compounds,
food additives, food components and carriers of phenolic antioxidants,
temperature, and other factors determine the antimicrobial activity of these
antioxidant phenolic compounds.
Origanum oil showed very effective antibacterial activity against C. jejuni
and C. sporogenes while thyme oil was very effective against C. jejuni.
Antimicrobial effects of origanum and thyme oil enhanced under low oxygen
tensions (Paster et aZ. 1990). Low oxygen tension might yield less oxidative
changes in the oils and/or anaerobic conditions might increase the sensitivity of
bacterial cells to the antimicrobial activity of the oils. The presence of an
oxygenated function in the monoterpene and their carbonylated products showed
significantly high antibacterial and antifungal activity (Naigre et al. 1996). The
antimicrobial activity of thyme oil or thymol against S. aureus and S.
Typhimurium was greater under anaerobic than aerobic conditions. Thymol and
carvacrol (phenols) are the main antimicrobial constituents of thyme oil (Juven
et al. 1994) while p-cymene and y-terpinene (terpenes) did not show any
antimicrobial activity S. Typhimurium.
Essential oils or their active compounds containing hydroxyl group (-OH)
are highly antimicrobial (Farag et al. 1989b). The presence of aromatic nucleus
with a polar functional group determines the inhibitory properties of the essential
oils. A hydroxyl group is much more effective compared to a carbonyl group.
The hydroxyl group can easily bind the active site of enzymes and alter their
metabolism. Inhibitory effects of the oils on the growth of S. cerevisiae followed
the similar pattern to that of Gram-positive bacteria. In general primary alcohols
exhibited higher antifungal activity than secondary and tertiary alcohols. The
antifungal activity of eugenol (4-allyl-guaiacol) was much higher than other
potent antifungal phenolic compounds such as cresol (4-methylphenol) and
guaiacol (o-methoxyphenol) (Kurita er al. 1981).
Besides the presence of the hydroxyl group in the phenolic structure, its
position in the phenolic ring strongly influences the microbial effectiveness of
components. The alkyl substitution into phenolic compound increases the
antimicrobial activity (Pelczar et al. 1988). Pauli and Knobloch (1987) reported
that o- and p-alkyl substituted phenols from spice essential oils exhibited strong
antifungal activity against 5 Aspergillus spp., 4 Penicillium spp. and 2 Fusarium
SPP.
Phenolic compounds in essential oils impair enzymatic mechanisms for
energy production and cellular component synthesis (Conner and Beuchat
1984b). It has been theorized that phenolic compounds are involved in multiple
mode of action for their antimicrobial activity. These compounds interact with
the cell membrane causing leakage of cellular components, change fatty acid and
phospholipid constituent, impair energy metabolism, alter nutrient uptake and
electron transport, and influence genetic material synthesis (Nychas 1995),
Phenolic compounds inhibit the cytoplasmic membrane-bound ATPase activity
in S. aureus (Ruco-Munoz et al. 1987). Essential oils of spices damage the
structural and metabolic enzymes, and inhibit repair of heat-injured yeasts
(Conner and Beuchat 1984b).
The chemical structure of the major component of the oil and its antifungal
properties are interrelated. Aromatic nucleus containing a polar functional group
enhanced the inhibitory properties of oils. Borneo1 and thujone possessed little
antifungal activity compared to thymol, which contains an aromatic nucleus. The
hydrophilic/lipophilic balance, presence of a phenolic -OH group that can easily
react and form hydrogen bonds with enzymes and other factors could also
determine the extent of the inhibition of essential oils (Farag et al. 1989b). The
presence and location of hydroxyl group on the molecule, the lipid solubility and
the degree of steric hindrance also determines the antimicrobial activity of
phenolic antioxidants (Raccach 1984).
Phenolic compounds containing conjugated ring structures and hydroxyl
groups scavenge and stabilize free radicals, and phenolic compounds containing
the carboxylic acid groups inhibit the lipid oxidation by metal chelation (Decker
1995).
The alkylation has been theorized to change the distribution ratio of the
aqueous and the nonaqueous phases by reducing the surface tension. The
presence of an acetate moiety enhances the activity of the related compound. For
example, the geranyl acetate showed a stronger antimicrobial activity against the
test microorganisms compared to geraniol. A similar result was reported in the
comparison of bornyl acetate to bomeol (Dorman and Deans 2000).
Kurita et al. (1981) examined the antifungal activity of some 40 kinds of
aliphatic and aromatic aldehydes, alcohols, phenols, ethers and hydrocarbons
from plant essential oils and some other related compounds against seven fungi
species. Cinnamaldehyde had the highest antifungal activity among aliphatic
aldehydes followed by perillaldehyde and citral. Aliphatic aldehydes with one
or more double bonds conjugated to their carbonyl group had much higher
antifungal activity than those that did not have double bonds. Antifungal activity
of p-methylbenzaldehyde was intermediate while benzaldehyde was very weak.
The inhibitory effect of the aldehydes, cinnamaldehyde, perillaldehyde, citral
and citronellal reduced in the presence of cysteine or glutathione indicating that
the antifungal inhibition is mainly due to the reaction of aldehydes with -SH
groups from fungi. The antifungal activity of the aldehydes is related to the
energy of the lowest empty molecular orbitals. Antifungal activity of aldehydes
was related to the energy level of the lowest empty molecular orbital. The lower
energy level of the orbital gives the molecule the higher antifungal activity.
Perillaldehyde, cinnamaldehyde, and citral are good electron acceptors. They
form charge transfer complexes with tryptophan, a good electron donor. The
strong antifungal or antimicrobial activity of aldehydes is possible due to their
ability to react with -SH groups and form charge transfer complexes with
electron donor molecules (Kurita er al. 1979).
The antifungal activity of a-and &unsaturated aliphatic aldehydes (such as
cinnamaldehyde, perillaldehyde and citral), and primary alcohols (such as
citronellol, geraniol, perillalcohol and 1-decanol) were very high. Antifungal
activity of 01, /3-saturated aliphatic aldehydes (such as citronellal, decanal),
secondary alcohols (such as L-menthol, borneol), and tertiary alcohols (such as
linalool and terpinol) were intermediate. The hydrocarbons, however, had very
low antifungal activity (Kurita and Koike 1982b).
The type of alkyl substituent in a nonphenolic ring structure affects the
antimicrobial activity. An alkenyl substituent (-CH =CH-) as in limonene
resulted in increased antimicrobial activity compared to an alkyl substituent
(-C =C-) as in p-cymene (Dorman and Deans 2000). Gram-negative bacteria are
more sensitive to alkylation and allylic side chains increases the antimicrobial
effect of component (Pelczar er al. 1988; Dorman and Deans 2000). The
stereochemistry influences the antimicrobial activity of compounds. The 0
isomers, rrans-isomers have been found to be more active compared to CY
isomers and cis-cis isomers. The compounds with methyl-isopropyl cyclohexane
rings and unsaturated cyclohexane rings are the most active compounds (Hinou
et al. 1989; Dorman and Deans 2000).
The presence of alkyl group(s) on benzene ring of phenol or guaiacol
enhanced the antifungal activity of these compounds. Compounds with the larger
size of alkyl group had the higher antifungal activity. Antifungal activity of ether
compounds enhanced with methyl group. The activity of methyl-eugenol and
methyl-isoeugenol was potent compared to that of eugenol and isoeugenol.
Antifungal activity of hydrocarbons tested was very weak (Kurita er al. 1981).
Antimicrobial activity of essential oil against microorganisms involves
different modes of action depending on major components of the oils. Bioactive
compounds interact with phospholipid bilayer of the cell membrane causing
leakage of cellular materials (Kim er al. 1995a; Juven er al. 1994), inactivation
of metabolic enzymes (Farag er al. 1989b) or damage to DNA. Wendakoon and
Sakaguchi (1995) reported that cinnamaldehyde inhibits amino acid
decarboxylase enzyme activity.
The lipophilic properties of terpenoids from essential oils, reactivity of their
functional groups and their aqueous solubility determines the microbial activity.
The antimicrobial activity of terpenes from essential oils against bacteria (e.g.,
P. vulgaris, E. aerogenes, E. coli, Rhodopseudomonas sphaeroides, and S.
aureus), and fungi (e.g., A . flavus, A . parasiticus, Penicillium rogueforti, and
Fusarium graminearum) was related to the water solubility of essential oils.

Essential oils damaged biological membrane interfering with membrane-
integrated enzymes (Knobloch e? al. 1989). Their site of action at the
phospholipid bilayers of the cells inhibits the electron transport, protein
translocation, phosphorylation and other enzymatic reactions. Cell wall
lipopolysaccharide of Gram-negative bacteria inhibits the penetration of
antimicrobial agents, and their attachment to DNA that causes the death of cells.
However, this trend is not always true since B. thermosphacta was as resistant
as S. liquefaciens (Ouattara e? al. 1997) and L. monoqtogenes was more
resistant to 11 essential oils than E. coli, E. coli 0157:H7, S. Typhimurium and
V. vulnificus (Kim et al. 1995a).
Alcoholic compounds have bactericidal activity. The alcohol terpenoids
showed antimicrobial activity against the test microorganisms acting as protein
denaturing, solvents or dehydrating agents. Aldehydes have strong antimicrobial
activity. An aldehyde group that conjugates to a carbon-carbon double bond
(-C = C-) has a high electronegativity arrangement (Moleyar and Narasimham
1986). An increase in electronegativity enhances the antimicrobial activity of the
compound (Kurita et al. 1979). These electronegative compounds interfere with
crucial electron transfer process and react with proteins, and nucleic acid
causing the inhibition of microbial growth (Donnan and Deans 2000). Ethanol
extract of cinnamon, nutmeg and allspice strongly inhibited the histidine, lysine
and ornithine decarboxylase activity of E. uerogenes. Presence of salt (NaCl)
further significantly enhanced inhibitory action of these essential oils on
decarboxylase activity. Cinnamaldehyde and eugenol components of the spices
were found to be strong inhibitors (Wendakoon and Sakaguchi 1995).
Inhibitory mechanism of phenolic antioxidants on microorganisms has been
found to be disruptive to the function and composition of cellular membrane, the
synthesis of DNA, RNA, protein and lipid, and the function of the
mitochondrion (Raccach 1984).
Allicin, the principle antibacterial compound in garlic, acts as an inhibitor
towards -SH group enzymes (Beuchat and Golden 1989). Allicin affects fatty
acids, lipid biosynthesis and RNA synthesis of microorganisms. Allicin inhibited
acetyl-CoA synthetase in fatty acid biosynthesis in plants, yeasts and mammals.
Bacterial acetate kinase and phosphotransacetylase enzyme systems were also
inhibited by allicin. Inhibition was dose dependent and allicin reversibly bonded
to enzymes forming non-covalent bonds (Focke e?al. 1990). The aqueous garlic
extract affected the structure and integrity of the outer surface of Cundida
albicans. The aqueous garlic extract damaged the yeast cell envelope and caused
the loss of intracellular components and morphological changes (Barone and
Tansey 1977; Ghannoum 1988). Garlic affected polar, nonpolarlipids, and fatty
acid content in yeast. The total lipid content decreased, higher proportions of
phosphatidylserines and lower proportions of phosphatidylcholines were found.
Oxygen consumption of the cells was reduced. Free sterols, sterol esters and
esterified steryl glycosides were accumulated in the cells. Palmitic acid and oleic
acid increased while linoleic and linolenic acid were decreased. Garlic interacted
with thiol groups in the essential proteins caused inactivation of enzymes and
inhibition of cellular growth (Ghannoum 1988). Adetumbi ef al. (1986) reported
that garlic extract interfered with enzymes in lipid biosynthesis.
Among six fractions (fractions A, B, C and D, allicin, and ajoene) derived
from garlic, ajoene had the strongest antifungal activity and inhibited the growth
of A . niger and C. albicans at less than 20 pg/mL. Ajoene-treated A . niger had
several morphological changes including disappearance of surface ornaments,
thinning of cell wall, detachment of cell membrane and cell wall, surface
depression of hypha, and destruction of cell organella. Although ajoene did not
exhibit antibacterial activity so far, it possessed a superior antifungal activity
compared to allicin, a strong antibacterial compound (Yoshida er al. 1987).
SYNERGISM
Synergy is the interaction of the compounds and/or factors in such a way

that the activity of individual compounds or factors is increased when they are
applied together. Compounds in the mixtures of spices and herbs have shown to
have synergistic activity. Although the amount of spices in food systems may not
always be enough to produce antimicrobial effect, when combined with intrinsic
factors such as pH and extrinsic factors such as temperature they may exert
antimicrobid activity.
The use of spices with other food ingredients such as sodium chloride,
sugar and organic acids, and also with thermal processing might provide a
synergistic effect in controlling microbial growth (Shelef er al. 1980; Giese
1994b). For example, heat stress may cause cellular membrane damage,
impairment to or lesions in the cytoplasmic membrane that allows essential oils
to move rapidly into the interior of the cells. The essential oils then impair the
metabolic functions and interfere with the recovery metabolism of injured cells
by their specific mode of actions. Essential oils had lethal effects on heat injured
yeast cells.
Ismaiel and Pierson (1990a) reported that origanum oil (100-200 ppm)
inhibited the growth of Clostridium botulinum and the inhibition increased
synergistically with sodium nitrite. In meat samples a combination of sodium
nitrate at 50-100 ppm and origanum oil at 400 ppm showed significant
antimicrobial activity.
Use of spice blends such as “chili powder” (red pepper, onion, paprika,
garlic, cumin and oregano) and “oriental five” (pepper, cinnamon, anise, fennel
and cloves) in food produces powerful antimicrobial effects. Spice extracts are
used to flavor and preserve many foods. Spices used in sausage making when
combined with organic acids (citric acid, acetic acid), salt and heating show
stronger antimicrobial effects (Kurita and Koike 1982a, b; Ziauddin et al. 1996).
In 1943, Blum and Fabian observed that the use of mustard oil inhibited A .
aceti, Saccharomyces ellipsoideus, S. cerevisiae. and Mycodennu vini in pickles
and sauerkraut (Shelef 1984).
Although lemon and lime juice possess very little antimicrobial activity,
they enhance the antibacterial effects of other spices synergistically. In acidic
environments the synergistic effect of lemon juice (citric acid) was higher
because of higher amount of its undissociated form. Essential oils at such low
pH dissolve in and/or attach to the lipid phase of the bacterial membrane (Juven
er al. 1994; Skandamis and Nychas 2000).
Synergistic effects of plant essential oils with low pH value (Juven et al.
1994; Tassou er al. 1995) and sodium chloride (Kurita and Koike 1982a, b) have
been reported. The combination of anise oil (0.1% v/v) with low pH (pH .4.2)
and salt (5% sodium chloride) showed a synergistic effect against Lactobacillus
curvatucus (Lachowicz et al. 1998). Sodium chloride alone exhibited very small
inhibitory effect against A . flavus, A . niger, G. candidum, Mucor spp., P.
roqueforti and Penicillium spp. but the combination of oregano and sodium
chloride showed a synergistic effect. Oregano essential oil, thymol and carvacrol
exhibited greater inhibition than sorbic acid at same concentrations (Akgul and
Kivanc 1988).
Tassou et al. (1995) evaluated the synergism of mint essential oil (0.5, 1.0,
1.5, and 2.0% w/w) and pH against L. monocytogenes and S. ententidis in food
model systems (tzatziki, tatmosalata and pate) at two different storage
temperatures (4 and 1OC). Mint essential oil exhibited the most antibacterial
effect in low pH systems (tzatziki pH 4.5) followed by relatively less acidic food
(taramosalata pH 5.0). However, no antimicrobial activity was observed in a
food system with neutral pH (pate pH 6 . 8 ) (Tassou et al. 1995). In general, S.
Enteritidis was more susceptible than L. monocytogenes and the difference was
higher at 1OC than 4C. Antimicrobial activity of mint essential oil increased with
the increase in the amount of essential oil.
ANTIOXIDANT PROPERTIES OF SPICES
The components of sage and rosemary have strong antioxidant activity.

Ginger and garlic scavenge hydroxyl radicals (OH] and react with
hypochlorous acid (HOCl) (Aruoma ez al. 1997). Barbut er al. (1988) compared
the antioxidative activity of rosemary oleoresin (200 ppm) to a commercial
mixture of butylated hydroxyanisole (BHA), butylated hydroxytoiuene (BHT)
(200 ppm) and citric acid in frozen and freeze dried breakfast sausages prepared
with 18% mechanically deboned turkey meat (MDTM). Rosemary oleoresin was
comparable to a commercial mixture of BHA, BHT and citric acid in freeze-
dried sausages for inhibition of lipid oxidation. Although commercial
antioxidants were more effective inhibiting of lipid oxidation in frozen sausages,
rosemary oleoresins significantly reduced lipid oxidation compared to control
samples with no antioxidants (Barbut et al. 1988). Rosemary oleoresin was
comparable to a mixture of BHA, BHT and citric acid in inhibition of lipid
oxidation in breakfast sausage prepared with 25 % MDTM at refrigeration
temperature (4C) for two weeks (Barbut et al. 1985).
Lopez-Bote et al. (1998) reported that the meat from broilers fed on a diet
containing 500 mg/kg rosemary and sage extracts had lower amounts of lipid
and cholesterol oxidation products than control samples. Both white and dark
meat samples had lower lipid and cholesterol oxidation products during
refrigerated and frozen storage. White and dark meat stored frozen for 4 months
and cooked to an internal temperature of 70C for 30 min and stored under
refrigeration conditions had lower oxidation products.
REFERENCES
ABDOU, I.A., ABOU-ZEID, A.A., EL-SHERBEENY, M.R. and ABOU-EL-

GHEAT, Z.H. 1972. Antimicrobial activities Allium sativum, Allium cepa,
Raphanus sativus, Capsicumfrutescens, Eruci sativa, and Allium kurrat on
bacteria. Qual. Plant. Mater. Veg. 22, 29-35.
ADETUMBI, M., JAVOR, G.T. and LAU, B.H. 1986. Allium sativum (garlic)
inhibits lipid biosynthesis by Candida albicans. Antimicrob. Agents
Chemother. 30, 499-501.
AKGUL, A. and KIVANC, M. 1988. Inhibitory effects of selected Turkish
spices and oregano components on some foodborne fungi. Intern. J. Food
Microbiol. 6, 263-268.
AKTUG, S.E. and KARAPINAR, M. 1986. Sensitivity of some common food
poisoning bacteria to thyme, mint, and bay leaves. Intern. J. Food
Microbiol. 3, 349-354.
AL-DELAIMY, K.S. and ALI, S.H. 1970. Antibacterial action of vegetable
extracts on the growth of pathogenic bacteria. J. Sci. Food Agric. 21,
110-1 12.
ARRAS, G. and GRELLA, G.E. 1992. Wild thyme, Thymus capitatus, essential
oil seasonal changes and antimycotic activity. J. Hort. Sci. 67, 197-202.
ARUOMA, O.I., SPENCER, J.P.E., WARREN, D., JENNER, P., BUTLER,
J. and HALLIWELL, B. 1997. Characterization of food antioxidants,
illustrated using commercial garlic and ginger preparations. Food Chem.
60, 149-156.
AZZOUZ, M.A. and BULLERMAN, L.B. 1982. Comparative antimycotic

effects of selected spices, plant components and commercial antifungal
agents. J. Food Prot. 45, 1298-1301.
BAHK, J., YOUSEF, A.E. and MARTH, E.H. 1990. Behavior of Listena
monocytogenes in the presence of selected spices. Lebensm.-Wiss. u.-
Technol. 23, 66-69.
BALENTINE, D.A., ALBANO, M.C. and NAIR, M.G. 1999. Role of
medicinal plants, herbs, and spices in protecting human health. Nutr. Rev.
57, S41-S45.
BARANOWSKI, J.D., DAVIDSON, P.M., NAGEL, C.W. and BRANEN,
A.L. 1980. Inhibition of Saccharomyces cerevisiae by naturally occurring
hydroxycinnamates. J . Food Sci. 45, 592-594.
BARBUT, S., DRAPER, H.H. and HADLEY, M. 1988. Effects of freezing
method and antioxidant on lipid oxidation in turkey sausage. J. Food Prot.
51, 878-882.
BARBUT, S., JOSEPHSON, D.B. and MAURER, A.J. 1985. Antioxidant
properties of rosemary oleoresin in turkey sausage. J. Food Sci. 50,
1356- 1359.
BARONE, F.E. and TANSEY, M.R. 1977. Isolation, purification,
identification, synthesis, and kinetics of activity of the anticandidal
component of Allium sativum, and a hypothesis for its model of action.
Mycologia 6, 793-825.
BASILICO, M.Z. and BASILICO, J.C. 1999. Inhibitory effects of some spice
essential oil on Aspergillus ochraceus NRRL 3 174 growth and ochratoxin
A production. Lett. Appl. Microbiol. 29, 238-241.
BAYOUMI, S . 1992. Bacteriostatic effect of some spices and their utilization
in the manufacture of yoghurt. Chem. Mikrobiol. Technol. Lebensm. 14,
21-26.
BECKSTROM-STERNBERG, S.M. and DUKE, J.A. 1994. Potential for
synergistic action of phytochemicals in spices. In Spices, Herbs and Edible
Fungi, (G. Charalambous, ed.) pp. 201-223, Elsevier, New York.
BELAICHE, T., TANTAOUI-ELARAKI, A. and IBRAHIMY, A. 1995.
Application of two levels factorial design to the study of the antimicrobial
activity of three terpenes. Sci. Aliment 15, 571-578.
BENJILALI, B., TANTAOUI-ELARAKI, A., AYADI, A. and IHLAL, M .
1984. Method to study antimicrobial effects of essential oils: Application
to the antifungal activity of six Moroccan essences. J. Food Prot. 47,
748-752.
BEUCHAT, L.R. 1976. Sensitivity of Vibrio parahaernolyticus to spices and
organic acids. J. Food Sci. 41,899-902.
BEUCHAT, L.R. 1994. Antimicrobial properties spices and their essential oils.
In Natural Antimicrobial System and Food Preservation, (V.M. Dillon and
R.G. Board, eds.) pp. 167-179, CAB International, Wallingford, UK.
BEUCHAT, L.R. and BARACKETT, R.E. 1990. Inhibitory Effects of Raw
carrots on Listeria monocytogenes. Appl. Environ. Microbiol. 56,
1734-1742.
BEUCHAT, L.R. and GOLDEN, D.A. 1989. Antimicrobials occurring
naturally in foods. Food Technol. 43, 134-142.
BILLING, J. and SHERMAN, P.W. 1998. Antimicrobial functions of spices:
why some like it hot. Q. Rev. Biol. 73, 3-49.
BLOCK, E. 1985. The chemistry of garlic and onions. Sci. Am. 252, 114-1 19.
BOONCHIRD, C. and FLEGEL, T.W. 1982. In vitro antifungal activity of
eugenol and vanillin against Candida albicans and Cryptococcus
neofomuzns. Can. J. Microbiol. 28, 1235-1241.
BRANEN, A.L., DAVIDSON, P.M. and KATZ, B. 1980. Antibacterial
properties of phenolic antioxidants and lipids. Food Technol. 34, 42, 44,
46, 51-53, 63.
BRIOZZO, J., NUNEZ, L., CHIRIF, J . , HERSZAGE, L. and D’AQUINO,
M. 1989. Antimicrobial activity of clove oil dispersed in a concentrated
sugar solution. J. Appl. Bacteriol. 66, 69-75.
BUCHANAN, R.L. and SHEPHERD, A.J. 1981. Inhibition of Aspergillus
parasiticus by thymol. J. Food Sci. 46, 976-977.
BULLERMAN, L.B. 1974. Inhibition of Aflatoxin production by cinnamon. J .
Food Sci. 39, 1163-1165.
CARSON, C.F., COOKSON, B.D., FARRELLY, H.D. and RILEY, T.V.
1995. Susceptibility of methicillin-resistant Staphylococcus aureus to the
essential oil of Melaleuca altemifolia. J. Antimicrob. Chemoth. 35,
42 1-424.
CARSON, C.F., HAMMER, K.A. and RILEY, T.V. 1996. In vitro activity of
the essential oil of Melaleuca altemifolia against Streptococcus spp. J.
Antimicrob. Chemoth. 37, 1177-1 181.
CARSON, C.F. and RILEY, T.V. 1995. Antimicrobial activity of the major
components of the essential oil of Melaleuca altemifolia. J. Appl. Bacteriol.
78, 264-269.
CERRUTTI, P. and ALZAMORA, S.M. 1996. Inhibitory effects of vanillin on
some food spoilage yeasts in laboratory media and fruit puree. Intern. J.
Food Microbiol. 29, 379-386.
CHANG, S.S., OSTRIC-MATIJASEVIC, B., HSIEH, O.A.L. and HUANG,
C.L. 1977. Natural antioxidants from rosemary and sage. J. Food Sci. 42,
1102-1 106.
CHI, S.P. and CHEN, T.C. 1992. Predicting optimum monosodium glutamate
and sodium chloride concentrations in chicken broth as affected by spice
addition. J. Food Processing Preservation 16, 313-326.
CLARK, W.R.E. 1970. Modem trends in the application of spices. Food
ManUf. 45, 53-54.
COLLINS, M.A. and CHARLES, H.P. 1987. Antimicrobial activity of
Carnosol and Ursolic acids: two anti-oxidant constituents of Rosmarimus
oficinalis L. Food Microbiol. 4, 311-315.
CONNER, D.E. 1993. Naturally occurring compounds. In Antimicrobials in
Foods, (P.M. Davidson and A.L. Branen, eds.) pp. 441-468, Marcel
Dekker, New York.
CONNER, D.E. and BEUCHAT, L.R. 1984a. Effect of essential oils from
plants on growth of food spoilage yeasts. 1. Food Sci. 49, 429-434.
CONNER, D.E. and BEUCHAT, L.R. 1984b. Sensitivity of heat-stressed
yeasts to essential oils of plants. Appl. Environ. Microbiol. 47, 229-233.
COSENTINO, S. et al. 1999. In vitro antimicrobial activity and chemical
composition of Sardinian Z’hymus essential oils. Lett. Appl. Microbiol. 29,
130- 135.
CRESPO, M.E., HIMENEZ, J., GOMIS, E. and NAVARRO, C. 1990.
Antibacterial activity of the essential oil of Thymus selpylloides subspecies
gadorensis. Microbios 61, 181-184.
CRUZ, T., CABO, M.P., CABO, M.M., JIMENEZ, J., CABO, J. and RUIZ,
C. 1989. In vitro antibacterial effect of the essential oil of Thymus
longij’lorus boiss. Microbios 60, 59-61.
CUTTER, C.N. 2000. Antimicrobial effect of herb extracts against Escherichia
coli 0157:H7, Listeria monocytogenes, and Salmonella typhimurium
associated with beef. J. Food Prot.. 63, 601-607.
CUVELIER, M.E., BERSET, C. and RICHARD, H. 1996. Antioxidative
activity and phenolic composition of pilot-plant and commercial extracts of
sage and rosemary. J. Am. Oil Chem. SOC.73, 645-652.
DAOUK, R.K., DAGHER, S.M. and SATTOUT, E.J. 1995. Antifingal
activity of the essential oil of Origanum syriacum L. J. Food Prot. 58,
1 147- 1 149.
DAVIDSON, P.M., POST, L.S., BRANEN, A.L. and MCCURDY, A.R.
1983. Naturally occurring and miscellaneous food antimicrobials. In
Antimicrobials in Food, (A.L. Branen and P.M. Davison, eds.) pp.
371-419, Marcel Dekker, New York.
DEANS, S.G. and RITCHIE, G. 1987. Antibacterial properties of plant
essential oils. Intern. J. Food Microbiol. 5, 165-180.
DEANS, S.G. and SVOBODA, K.P. 1988. Antibacterial activity of French
tarragon (Arfemisia dracunculus Linn.) essential oil and its constituents
during ontogeny. J. Hort. Sci. 63, 505-508.
ANTIMICROBIAL ACTTVITY OF SPICES 41
DECKER, E.A. 1995. The role of phenolics, conjugated linoleic acid,

carnosine, and pyroloquinoline quinoe as nonessential dietary antioxidants.
Nutr. Rev. 53, 49-58.
DEIBEL, K.E. and BANWART, G.J. 1984. Effects of spices on Campylobacter
jejuni at three temperatures. J. Food Safety 6, 241-251.
DICKENS, J.A., BERRANG, M.E. and COX, N.A. 2000. Efficacy of an
herbal extract on the microbiological quality of broiler carcasses during a
simulated chill. Poultry Sci. 79,1200-1203.
DORMAN, H.J.D. and DEANS, S.G. 2000. Antimicrobial agents from plants:
antibacterial activity of plant volatile oils. J . Appl. Microbiol. 88, 308-316.
DUKE, J.A. 1994. Biologically active compounds in important spices. In
Spices, Herbs and Edible Fungi, (G. Charalambous, ed.) pp. 225-250,
Elsevier, New York.
EL-KADY, I.A., EL-MARAGHY, S.S. and MOSTAFA, M.E. 1993.
Antibacterial and antidemtophyte activities of some essential oils from
spices. Qatar Univ. Sci. J. 13, 63-69.
EL-KHATEIB, T. and EL-RAHMAN, H.A. 1987. Effect of garlic and
Luctobacillus plantarum on growth of Salmonella typhimurium in Egyptian
fresh sausage and beef burger. J. Food Prot. 50, 310-31 1.
FARAG, R.S., DAW, Z.Y. and ABO-RAYA, S.H. 1989a. Influences of some
spice essential oils on Aspergillus parasiticus growth and production of
aflatoxins in synthetic medium. J. Food Sci. 54, 74-76.
FARAG, R.S., DAW, Z.Y., HEWEDI, F.M. and EL-BAROTY, G.S.A.
1989b. Antimicrobial activity of some Egyptian spice essential oils. J. Food
Prot. 52, 665-667.
FARBOOD, M.I., MACNEIL, J.H. and OSTOVAR, K. 1976. Effects of
rosemary spice extractive on growth of microorganisms in meats. J. Milk
Food Technol. 39, 675-679.
FARRELL, K.T. 1985. Spices, Condiments, and Seasonings. AVI Publishing
Co., Westport, CT.
FOCKE, M., FELD, A. and LICHTENTHALER, H.K. 1990. Allicin, a
naturally occurring antibiotic from garlic, specifically inhibits acetyl-CoA
synthetase. FEBS Lett. 262, 106-108.
FRAENKEL, G.S. 1959. The raison d’Etre of secondary plant substances.
Science. 129, 1466-1470.
FREEMAN, G.G. and WHENHAM, R.J. 1975. Survey of volatile components
of some Allium species in terms of S-alky-(en)-yl BL- cysteine sulphoxides
present as flavour precursors. J. Sci. Food Agric. 26, 1869-1886.
GANDI, D.N. and GHODEKAR, D.R. 1988. Antibacterial activity of garlic
extract against lactic acid bacteria and contaminants of fermented milks.
Indian J. Dairy Sci. 41, 511-512.
GHANNOUM, M.A. 1988. Studies on the anticandidal mode of action of

Allium sativum (garlic). J. Gen. Microbiol. 134, 2917-2924.
GIESE, J . 1994a. Antimicrobials: assuring food safety. Food Technol. 48,
101-1 10.
GIESE, J . 1994b. Spices and seasoning blends: a taste for all seasons. Food
Technol. 48(4), 87-90, 92, 94-95, 98.
HALL, M.A. and MAURER, A.J. 1986. Spice extracts, lauricidin, and
propylene glycol as inhibitors of Clostndium botulinum in turkey frankfurter
slurries. Poultry Sci. 65, 1167-1 171.
HAO, Y.Y., BRACKETT, R.E. and DOYLE, M.P. 1998a. Efficacy of plant
extracts in inhibiting Aeromonas hydrophila and Listeria monocytogenes in
refrigerated, cooked poultry. Food Microbiol. 15, 367-378.
HAO, Y.Y., BRACKETT, R.E. and DOYLE, M.P. 1998b. Inhibition of
Listena monocytogenes and Aeromonas hydrophila by plant extracts in
refrigerated cooked beef. J . Food Prot. 61, 307-312.
HARGREAVES, L.L., JARVIS, B., RAWLINSON, A.P. and WOOD, J.M.
1975. The antimicrobial effects of spices, herbs and extracts from these and
other food plants. Sci. Tech. Surveys, Brit. Food Manuf. Ind. Res. Assoc.
88, 1-56.
HASSAN, C.M., AHSAN, M. and ISLAM, S.K.N. 1989. In vitro antibacterial
screening of the oils of Nigella sativa seeds. Bangladesh J. Botany 18,
171- 174.
HEFNAWY, Y.A., MOUSTAFA, S.I. and MARTH, E.H. 1993. Sensitivity of
Listena monocytogenes to selected spices. J. Food Prot. 56, 876-878.
HILI, P., EVANS, C.S. and VENESS, R.G. 1997. Antimicrobial action of
essential oils: the effect of dimethylsulphoxide on the activity of cinnamon
oil. Lett. Appl. Microbiol. 24, 269-275.
HINOU, J.B., HARVALA, C.E. and HINOU, E.B. 1989. Antimicrobial
activity screening of 32 common constituents of essential oils. Pharmazie
44, H4.
HITOKOTO, H . , MOROZUMI, S . , WAUKE, T., SAKAI, S. and KURATA,
H. 1980. Inhibitory effects of spices on growth and toxin production of
toxigenic fungi. Appl. Environ. Microbiol. 39, 818-822.
HUGHES, B.G. and LAWSON, L.D. 1991. Antimicrobial effects of Allium
sativum L. (garlic), Allium ampeloprasum L. (elephant garlic), and Allium
cepa L. (onion), garlic compounds and commercial garlic supplement
products. Phytother. Res. 5, 154-158.
HUHTANEN, C.N. 1980. Inhibition of Clostridium botulinum by spice extracts
and aliphatic alcohol. J. Food Prot. 43, 195-196.
ISLAM, S.K.N, AHSAN, M., FERDOUS, A.J. and FAROQUE, A.B.M.
1990. In vitro antibacterial activities of commonly used spices. Bangladesh
J . Botany 19, 99-101.
ISMAIEL, A.A. and PIERSON, M.D. 1990a. Inhibition of growth and

germination of Clostridium botulinum 33A, 40B, and 1623E by essential oil
of spices. J. Food Sci. 55, 1676-1678.
ISMAIEL, A.A. and PIERSON, M.D. 1990b. Effect of sodium nitrite and
origanum oil on growth and toxin production of Clostridium botulinu~iin
TYG broth and ground pork. J. Food Prot. 53, 958-960.
ISMAIL, S.A.S., DEAK, T., EL-RAHMAN, H.A.A., YASSIEN, M.A.M.
and BEUCHAT, L.R. 2000. Presence and changes in populations of yeasts
on raw and processed poultry products stored at refrigeration temperature.
Intern. J. Food Microbiol. 62, 113-121.
ISMAIL, S.A.S., DEAK, T., EL-RAHMAN, H.A.A., YASSIEN, M.A.M.
and BEUCHAT, L.R. 2001. Effectiveness of immersion treatments with
acids, trisodium phosphate, and herb decoctions in reducing populations of
Y. Iipolytica and naturally occurring aerobic microorganisms on raw
chicken. Intern. J. Food Microbiol. 64, 13-19.
JAY, J.M. 1996. Modern Food Microbiology. Chapman & Hall, New York.
JAY, J.M. and RIVERS, G.M. 1984. Antimicrobial activity of some food
flavoring compounds. J . Food Safety 6, 129-139.
JOHNSON, M.G. and VAUGHN, R.H. 1969. Death of Salmonella
typhimurium and Escherichia coli in the presence of freshly reconstituted
dehydrated garlic and onion. Appl. Microbiol. 17, 903-905.
JUVEN, B.J., KANNER, J . , SCHVED, F. and WEISSLOWICZ, H. 1994.
Factors that interact with the antibacterial action of thyme essential oil and
its active constituents. J. Appl. Bacteriol. 76, 626-631.
KARAPINAR, M. and AKTUG, A.E. 1987. Inhibition of foodborne pathogens
by thymol, eugenol, menthol, and anethole. Intern. J . Food Microbiol. 4,
161-166.
KIM, J.M., MARSHALL, M.R., CORNELL, J.A., PRESTON, J.F. and WEI,
C.I. 1995a. Antibacterial activity of carvacrol, citral, and geraniol against
Salmonella typhimurium in culture medium and on fish cubes. J. Food Sci.
60, 1364-1374.
KIM, J., MARSHALL, M.R. and WEI, C. 1995b. Antibacterial activity of
some essential oil components against five foodborne pathogens. J. Agric.
Food Chem. 43, 2839-2845.
KIVANC, M. and AKGUL, A. 1986. Antibacterial activities of essential oils
from Turkish spices and citrus. Flavour and Frag. J. I , 175-179.
KIVANC, M., AKGUL, A. and DOGAN, A. 1991. Inhibitory and stimulatory
effects of cumin, oregano, and their essential oils on growth and acid
production of Lactobacillus plantamm and Leuconostoc mesenteroides.
Intern. J. Food Microbiol. 13, 81-86.
50 E. CEYLAN and D . Y . C . FUNG
KNOBLOCH, K., PAULI, A., IBERL, B., WEIGAND, H. and WEIS, N.

1989. Antibacterial and antifungal properties of essential oil components.
3. Essent. Oil Res. I , 119-128.
KURITA, N. and KOIKE, S. 1982a. Synergistic antimicrobial effect of sodium
chloride and essential oil components. Agric. Biol. Chem 46, 159-165.
KURITA, N. and KOIKE, S. 1982b. Synergistic antimicrobial effect of acetic
acid sodium chloride and essential oil components. Agric. Biol. Chem 46,
1655- 1660.
KURITA, N. and KOIKE, S. 1983. Synergistic antimicrobial effect of ethanol,
sodium chloride, acetic acid and essential oil components. Agric. Biol.
Chem 47, 67-75.
KURITA, N., MIYAJI, M., KURANE, R. and TAKAHARA, Y. 1981.
Antifungal activity of components of essential oils. Agric. Biol. Chem. 45,
945-952.
KURITA, N., MIYAJI, M., KURANE, R., TAKAHARA, Y. and ICHIMRA,
K. 1979. Antifungal activity and molecular orbital energies of aldehyde
compounds from oils of higher plants. Agric. Biol. Chem. 43, 2365-2371.
LACHOWICZ, K.J. ef at. 1998. The synergistic preservative effects of the
essential oils of sweet basil (Ocimum basilicum L.) against acid tolerant
food microflora. SOC.Appl. Microbiol. 26, 209-214.
LANCASTER, J.E. and SHAW, M.L. 1989. Glutamyl peptides in the
biosynthesis of s-alk(en)yl-L-cysteine sulphoxides (flavour precursors) in
allium. Phytochemistry 28, 455-460.
LEISTNER, L. 1992. Food preservation by combined methods. Food Res.
Intern. 25, 151-158.
LEUNG, A.Y. and FOSTER, S . 1996. Encyclopedia of Common Natural
Ingredients Used in Food, Drugs and Cosmetics. John Wiley & Sons, New
York.
LEWIS, Y . S . 1984. Spices and Herbs for the Food Industry. Food Trade Press,
Orpington, England.
LIS-BALCHIN, M. and DEANS, S.G. 1997. Bioactivity of selected plant
essential oils against Listena monocytogenes. J. Appl. Microbiol. 82,
759-762.
LOPEZ-BOTE, C.J., GRAY, J.I., GOMAA, E.A. and FLEGAL, C.J. 1998.
Effects of dietary administration of oil extracts from rosemary and sage on
lipid oxidation in broiler meat. Brit. Poultry Sci. 39, 235-240.
MACNEIL, J.H., DIMICK, P.S. and MAST, M.G. 1973. Use of chemical
compounds and a rosemary spice extract in quality maintenance of deboned
poultry meat. J. Food Sci. 38, 1080-1081.
MACNEIL, J.H. and MAST, M.G. 1973. Frankfurters without nitrates or
nitrites. Food Prod. Dev. 7, 36, 38-40.
MADSEN, M.G. and GRYPA, R.D. 2000. Spices, flavor systems, the
electronic nose. Food Technol. 54, 44-46.
MAHMOUD, A.L. 1994. Antifungal action and antiaflatoxigenic properties of
some essential oil constituents. Lett. Appl. Microbiol. 19, 110-1 13.
MANDERFELD, M.M., SCHAFER, H.W., DAVIDSON, P.M. and
ZOTTOLA, E.A. 1997. Isolation and identification of antimicrobial
furocoumarins from parsley. J. Food Prot. 60, 72-77.
MANSOUR, E.H. and KHALIL, A.H. 2000. Evaluation of antioxidant activity
of some plant extracts and their application to ground beef patties. Food
Chem. 69, 135-141.
MARTH, E.H. 1966. Antibiotics in food - naturally occurring developed and
added. Residue Rev. 12, 65-161.
MENDOZA-YEPES, M.J., SANCHEZ-HIDALGO, L.E., MAERTENS, G.
and MARIN-INIESTA, F. 1997. Inhibition of Listeria rnonocytogenes and
other bacteria by a plant essential oil (Dmc) in Spanish soft cheese. J. Food
Safety 17, 47-55.
MOCHIZUKI, E.M. and YAMAMOTO, T. 1998. Identification of Allium
products using flame photometric detection gas chromatography and
distribution patterns of volatile sulfur compounds. J. Agric. Food Chem.
46, 5170-5176.
MOLAYER, V. and NARASIMHAM, P. 1986. Antifungal activity of some
essential oil components. Food Microbiol. 3, 33 1-336.
MOORE, G.S. and ATKINS, R.D. 1977. The fungicidal and fungistatic effects
of an aqueous garlic extract on medically important yeast like fungi.
Mycologia. 69, 341-348.
MOROZUMI, A. 1978. Isolation, purification, and antibiotic activity of
o-methoxy-cinnamaldehyde from cinnamon. Appl . Environ. Microbiol . 36,
577-583.
MOYLER, D.A. 1994. Spices - recent advances. In Spices, Herbs, und Edible
Fungi, (G. Charalombus, ed.) pp. 1-41, Elsevier, New York.
NADAL, N.G.M., MONTALVO, A.E. and SEDA, M. 1973. Antimicrobial
properties of bay and other phenolic essential oils. Cosmet. Perfumery 88,
37-38.
NAIDU, A.S., BIDLACK, W.R. and CRECELIUS, A.T. 2000. Flavonoids.
In Natural Food Antimicrobial Systems, (A.S. Naidu, ed.) pp. 325-348,
CRC Press, Boca Raton, FL.
NAIGRE, R., KALCK, P., ROQUES, C., ROUX, I. and MICHEL, G . 1996.
Comparison of antimicrobial properties monoterpenes and their
carbonylated products. Planta Med. 62, 275-277.
NAKATANI, N. 1994. Antioxidant and antimicrobial constituents of herbs and
spices. In Spices, Herbs and Edible Fungi, (G. Charalambous, ed.) pp.
251-271, Elsevier, New York.
NYCHAS, G.J.E. 1995. Natural antimicrobials from plants. In New Methods

of Food Preservation, (G.W. Gould, ed.) pp. 58-89, Blackie Academic
Professional, London.
ONAWUNMI, G. and OGUNLANA, E.O. 1986. A study of the antibacterial
activity of essential oil of lemon grass (Cymbopogon citratus). Intern. I .
Crude Drug Res. 24, 64-68.
OUATTARA, B., SIMARD, R.E., HOLLEY, R.A., PIETTE, G.J.-P. and
BEGIN, A. 1997. Antibacterial activity of selected fatty acids and essential
oils against six meat spoilage organisms. Intern. J. Food Microbiol. 37,
155- 162.
PANDIT, V.A. and SHELEF, L.A. 1994. Sensitivity oflistena monocytogenes
to rosemary (Rosmannus oflcinalis L.). Food Microbiol. 11, 57-63.
PARRY, J.W. 1969. Spices Vol. 1. Chemical Publishing Co., New York.
PASTER, N., JUVEN, B.J., SHAAYA, E., MENASHEROC, M., NIRZAN,
R., WEISSLOWLICZ, H. and RAVID, U. 1990. Inhibitory effect of
oregano and thyme essential oils on moulds and foodborne bacteria. Lett.
Appl. Microbiol. 11, 33-37.
PAULI, A. and KNOBLOCH, K. 1987. Inhibitory effects of essential oil
components on growth of food-contaminating fungi. Z. Lebensm. Unters.
For. 185, 10-13.
PELCZAR, M.J., CHAN, E.C.S. and KRIEG, N.R. 1988. Control of
microorganisms: the control of microorganisms by physical agents. In
Microbiology, pp. 469-509, McGraw-Hill Intern., New York.
PSZCZOLA, D. 1999. Engineering ingredients: Believe it or not. Food
Technol. 53(7), 98-105.
RACCACH, M. 1984. The antimicrobial activity of phenolic antioxidants in
foods: A review. J. Food Safety 6, 141-170.
RAMADAN, F.M., EL-ZANFALY, R.T., EL-WAKEIL, F.A. and ALIAN,
A.M. 1972. On the antibacterial effects of some essential oils: I. Use of
agar diffusion method. Chem. Mikrobiol. Technol. Lebensm. I, 96-102.
REES, L.P., MINNEY, S.F., PLUMMER, N.T., SLATER, J.H. and
SKYRME, D.A. 1993. A quantitative assessment of the antimicrobial
activity of garlic (Allium sativum). World J. Microbiol. Biot. 9, 303-307.
ROSENGARTEN, F. 1969. The book of spices. Livingston Publishing Co.,
Wynnewood, PA.
RUCO-MUNOZ, E., BARGIOTA, E.E. and DAVIDSON, P.M. 1987. Effects
of selected phenolic compounds on the membrane bound adenosine
triphosphate Staphylococcus aureus. Food Microbiol. 4 , 239-249.
RUSSELL, A.D. 1991. Mechanisms of bacterial resistance to non-antibiotics:
food additives and food and pharmaceutical preservatives. J. Appl.
Microbiol. 71, 191-201.
RUSSO, M., GALLETTI, G.C., BOCCHINI, P. and CARNACINI, A. 1998.

Essential oil chemical composition of wild populations of Italian oregano
spice (Origanurn vulgare ssp. Hirtum (Link) Ietswaart): a preliminary
evaluation of their use in chemotaxonomy by cluster analysis. 1.
Inflorescences. J. Agric. Food Chem. 46, 3741-3746.
SALMERON, J., JORDANO, R. and POZO, R. 1990. Antimycotic and
antiaflatoxigenic activity of oregano (Ongunurn vulgare, L.) and thyme
(Thymus vulgaris, L.). J. Food Prot. 53, 697-700.
SALZER, U.J. 1982. Antimicrobial action of some spice extracts and mixtures.
Fleischwirtschaft 62, 885-887.
SARKAR, S.K. and PHAN, C.T. 1979. Naturally occurring and ethylene-
induced phenolic compounds in the carrot root. J. Food Prot. 42, 526-534.
SATO, A., TERAO, M. and HONMA, Y. 1990. Antibacterial action of garlic
extract on food poisoning bacteria. J. Food Hyg. SOC.Jpn 3, 328-332.
SAXENA, A.P. and VYAS, K.M. 1986. Antimicrobial activity of seeds of
some ethnomedicinal plants. J. Econ. Taxon. Bot. 8, 291-299.
SCHULZ, H., KRUGER, H., LIEBMAN, J. and PETERKA, H. 1998.
Distribution of volatile sulfur compounds in a interspecific hybrid between
onion (Allium ceps L.) and leek (Alliurnporrum L.). J. Agric. Food Chem.
46, 5220-5224.
SHANKARANARAYANA, M.L., RAGHAVAN, B., ABTAHAM, K.O. and
NATARAJAN, C.P. 1974. Volatile sulfur compounds in food flavors.
CRC-Crit. Rev. Food Technol. 4, 395-435.
SHAPIRO, S . , MEIER, A. and GUGGENHEIM, B. 1994. The antimicrobial
activity of essential oils and essential oil components towards oral bacteria.
Oral Microbiol. Immun. 9, 202-204.
SHARMA, A., TEWARI, G.M., SHRIKHANDE, A.J., PADWAL-DESAI,
S.R. and BANDYOPADHYAY, C. 1979. Inhibition of aflatoxin-producing
fungi by onion extracts. J. Food Sci. 44, 1545-1547.
SHELEF, L.A. 1984. Antimicrobial effects of spices. J. Food Safety 6, 29-44.
SHELEF, L.A., JYOTHI, E.K. and BULGARELLI, M.A. 1984. Growth of
enteropathogenic and spoilage bacteria in sage-containing broth and foods.
J. Food Sci. 49, 737-740, 809.
SHELEF, L.A., NAGLIK, O.A. and BOGEN, D.W. 1980. Sensitivity of some
common foodborne bacteria to the spices sage, rosemary, and allspice. J.
Food Sci. 45, 1042-1044.
SHETTY, R.S., SINGHAL, R.S. and KULKARNI, P.R. 1994. Antimicrobial
properties of cumin. World J. Microbiol. Biot. 10, 232-233.
SHIBASAKI, I. 1982. Food preservation with nontraditional antimicrobial
agents. J. Food Safety 4, 35-58.
SIVROPOULOU, A., KOKKINI, S., LANARAS, T. and ARSENAKIS, M.

1995. Antimicrobial activity of mint essential oils. J. Agric. Food Chem.
43, 2384-2388.
SIVROPOULOU, A., NIKOLAOU, C., PAPANIKOLAOU, E., KOKKINI, S.,
LAMARAS, T. and ARSENAKIS, M. 1997. Antimicrobial, cytotoxic and
antiviral activities of Salviafructicosa essential oil. J. Agric. Food Chem.
45, 3197-3201
SIVROPOULOU, A., PAPANIKOLAOU, E., NIKOLAOU, C., KOKKINI, S.,
LANARAS, T. and ARSENAKIS, M. 1996. Antimicrobial and cytotoxic
activities of origanum essential oils. J. Agric. Food Chem. 44, 1202-1205.
SKANDAMIS, P.N. and NYCHAS, G.J. 2000. Development and evaluation of
a model predicting the survival of Eschen'chia coli 0157:H7 NCTC 12900
in homemade eggplant salad at various temperatures, pHs, and oregano
essential oil concentrations. Appl. Environ. Microbiol. 66, 1646-1653.
SMITH-PALMER, A., STEWART, J. and FYFE, L. 1998. Antimicrobial
properties of plant essential oils and essences against five important
foodborne pathogens. Lett. Appl. Microbiol. 26, 118-122.
SOMAATMADJA, D., POWERS, J.J. and HANDY, M.K. 1964.
Anthocyanins. V1. Chelation studies on anthocyanins and other related
compounds. J. Food Sci. 29, 655-660.
STECCHINI, M.L., SARAIS, I. and GIAVEDONI, P. 1993. Effect of essential
oils on Aeromonas hydrophila in a culture medium and in cooked pork. J.
Food Prot. 56, 405-409.
SURESH, P., INGLE, V.K. and VIAYALAKSHMI, V. 1992. Antibacterial
activity of eugenol in comparison with other antibiotics. J. Food Sci.
Technol. 29, 254-256.
TANSEY, M.R. and APPLETON, J.A. 1975. Inhibition of fungal growth by
garlic. Mycologia 67, 409-4 13.
TASSOU, C.C., DROSINOS, E.H. and NYCHAS, G.J.E. 1995. Effect of
essential oil from mint (Mentha pipenta) on Salmonella enteritidis and
Listen'a monocytogenes in model food systems at 4 and 10°C. J. Appl.
Bacteriol. 78, 593-600.
TING, W.T.E. and DEIBEL, K.E. 1992. Sensitivity of Listen'a monocytogenes
to spices at two temperatures. J. Food Safety 12, 129-137.
UEDA, S., YAMASHITA, H., NAKAJIMA, M. and KUWABARA, Y. 1982.
Inhibition of microorganisms by spice extracts and flavoring compounds.
J. Jpn. SOC.Food Sci. Technol. 29, 111-1 16.
UHL, S. 2000. Spices: tools for alternative or complementary medicine. Food
Technol. 54(5), 61-62, 64, 65.
WAN, J., WILCOCK, A. and CONVENTRY, M.J. 1998. The effect of
essential oils of basil on the growth of Aeromonas hydrophila and
Pseudomonas Juorescens. J. Appl. Microbiol. 84, 152-158.
WANG, M., KIKUZAKI, H., ZHU, N., SANG, S . , NAKATANI, N. and HO,
C. 2000. Isolation and structural elucidation of two new glycosides from
sage (Salvia o@icinalis L.). J. Agric. Food Chem. 48, 235-238.
WANG, M., LI, J., RANGARAJAN, M., SHAO, Y., LAVOIE, E.J.,
HUANG, T. and HO, C. 1998. Antioxidative phenolic compounds from
sage (Salvia officinalis). J. Agric. Food Chem. 46, 4869-4873.
WENDAKOON, C.N. and SAKAGUCHI, M. 1995. Inhibition of amino acid
decarboxylase activity of Enterobacter aerogenes by active components in
spices. J. Food Prot. 58, 280-283.
WILLIAMS, S.K. and BROWN, W.L. 1987. Future trends for flavoring and
spices. Food Technol. 41(6), 76, 78-79, 124.
WISEMAN, S.A., BALENTTINE, D.A. and FREI, B. 1997. Antioxidants in
tea. Cri. Rev. Food Sci. Nutr. 37, 705-718.
WU, J.W., LEE, M.H., HO, C.T. and CHANG, S.S. 1982. Elucidation of the
chemical structures of natural antioxidants isolated from rosemary. J. Am.
Chem. SOC.59, 339-345.
YOSHIDA, S., KADUGA, S . , HAYASHI, N., USHIROGUCHI, T.,
MATSUURA, H. and NAKAGWA, S. 1987. Antifungal activity of ajoene
derived from garlic. Appl. Environ. Microbiol. 53, 615-617.
ZAIKA, L.L. 1988. Spices and Herbs: Their antimicrobial activity and its
determination. J. Food Safety 9, 97-1 17.
ZIAUDDIN, K.S., RAO, H.S. and FAIROZE, N. 1996. Effect of organic acids
and spices on quality and shelf-life of meats at ambient temperature. J.
Food Sci. Technol. 33, 255-258.

Antimicrobial Activity of Spices

Uploaded by

Document Information

Original Title

Copyright

Available Formats

Share this document

Share or Embed Document

Sharing Options

Did you find this document useful?

Is this content inappropriate?

Copyright:

Available Formats

Antimicrobial Activity of Spices

Uploaded by

Copyright:

Available Formats

ANTIMICROBIAL ACTIVITY OF SPICES’

ERDOGAN CEYLAN and DANIEL Y. C. FUNG’

Food Science Institute

Extracts of plants, spices and herbs play an important role in promoting

Spices are primarily condiments used in cooking in modem life but in

USE OF SPICES IN FOOD

countries. Spices with strong antimicrobial activity such as garlic, onion,

75-100% Garlic, onion, allspice, oregano, thyme, cinnamon,

50-75 % Marjoram, mustard, caraway, mint, sage, fennel,

Less than 50 % Basil, parsley, cardamom, pepper (black and white)

'Adapted from Billing and Sherman 1998.

Spice Bacterial Species Bacterial Species Not References

Cumin Aerobacter aerogenes Klebsiella pneumoniae Azzouz and Bullerman 1982

Dill Acinefobacter calcoaceticus Alcaligenesfaecalis Deans and Ritchie 1987

Fennel Aerobacter aerogenes Alcaligenes faecalis Deans and Ritchie 1987

Lemongrass Bacillus ceretis Sireptococcusfaecaiis Onawunmi and Ogulana 1986

Mint Acinetobacter calcoaceticus Alcaligenesfaecabs Aktug and Karapinar 1986

Onion Escherichia coli None Abdou er al. 1972

Oregano A erobacter aerogenes None kuchat 1994

Spice Bacterial Species Bacterial Species Not References

Sage A erobacter aerogenes A cinetobacter calcoaceticus Auouz and Bullerman 1982

' Adapted from Billing and Sherman 1988.

Effect of temperature on the antimicrobial properties of spices is dubious.

distilled extraction at high temperature showed similar results. Oregano, sage

ANTIMICROBIAL PROPERTIES OF SPICES

Spices have been found to have antimicrobial activities against bacteria,

Allspice (pimento) Citronella Mandarin Peppermint

Almond (bitter) Clove Marjoram Rosemary

Angelica Coriander Musky bugle Sage

Basil (sweet) Dill Mustard Sassafras

Bay (laurel) Elecampane Nutmeg Spearmint

Bergamot Fennel Onion Star anise

Calrnus Garlic Orange Tarragon (estragon)

Cananga Ginger Oregano Thyme

Caraway Lemon Paprika Turmeric

Cardamom Licorice Parsley Verbena

Celery Lime Pennyroyal Wintergreen

* Adapted from Beuchat and Golden 1989

One of earliest studies on the antimicrobial activity of spices was reported

> 0.6 Onion, black pepper and white pepper

0.2-0.6 Garlic, capsicums, lemon, lime, and parsley

’ Adapted from Billing and Sherman 1998.

A large volume of data of antimicrobial activity of spices is available, but

(7) Gram-negative bacteria are more resistant than Gram-positive bacteria.

ANTIBACTERIAL PROPERTIES OF SPICES

Use of spices with antioxidant, antimicrobial, flavor enhancer and

Rosemary Cinnamon Thyme Oregano Bay

Garlic Cloves AlIspice Sage Vanilla

' Adapted from Duke 1994.

Antimicrobial activity Spice

Strong Cinnamon, clove, mustard

Medium Allspice, bay leaf, caraway, coriander, cumin, oregano, rosemary,

Weak Black pepper, red pepper, ginger

Adapted from Zaika 1988

(125 ppm) inhibited C. botulinum toxin production in turkey frankfurters (Hall

Black pepper 125 1 5.7 0120 0

White pepper 125 1 5.6 0/20 0

Bay leaf 125 1 5.8 0120 0

Nutmeg 125 1 5.9 0120 0

I Adapted from Hall and Maurer 1986.

yeast (Block 1985). Addition of as little as 1% (v/v) garlic extract completely

the minimum inhibitory concentration from 10 to 100 pg against Gram-positive,

furocoumarins isolated from all varieties of parsley inhibited the growth of E.