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Review Article
Department of Home Economics, New Mexico State University, P.O. Box 30003, Dept. 3470, Las Cruces, NM 88003
(U.S.A.)
'Received August 1, 1994; accepted September 6, 1994)
The populari~ of highly spiced cuisine and consumer demand fop" more flavolful foods which are also low in sodium and fat have
resulted in a continuing interest in the use of spices and herbs in food products. Although such condiments are generally used for the
aesthetic properties the3, contribute to food products, spices and herbs can often be a major source of microbial contamination. Studies
investigating bacterial and/or fungal contamination of spices and herbs are reviewed. The high levels of microbial contamination in
spices and herbs reported by many of the studies reviewed suggests a need for better control in all aspects of the production, processing
and usage of these products to prevent potential food spoilage and food-borne illnesses due to contaminated spices and herbs.
Introduction
Spices and herbs have been used for a variety of functions
for centuries. In ancient times, spices were so valuable that
they were used as a form of money and, for many years,
were so expensive that they were available only to the very
rich. Not only were the spices used to season foods, but they
were often used as perfumes, cosmetics and aphrodisiacs
(1). Ancient Greek, Roman and Chinese writings indicate
that spices were often used for medicinal purposes. The use
of spices and herbs for cosmetic and medicinal purposes is
still seen today.
Spices and herbs have also been used for centuries for the
aroma and flavor characteristics they provide to foods. In
ancient times, when food preservation was inadequate,
spices were used to Cover spoilage in food products. While
this is no longer an acceptable use of spices and herbs, the
increasing popularity of highly spiced cuisines as well as a
desire for flavorful foods which are low in sodium and fat
have sparked an increase in the use of spices and herbs (2).
Unfortunately, spices and herbs often contribute more than
aesthetic properties to foods. Many spices are grown and
harvested in poor sanitary conditions in areas abundant in
warmth and humidity. Such conditions lay the groundwork
for potential microbiological contamination. Numerous
studies have indicated high microbial loads in spices and
herbs which could pose a problem for food manufacturers.
0023-6438/95/010001 + 11 $08.00/0
Bacillus megaterium identified as the most common species. Lactobacillus was detected in all spices, while Streptococcus sp. was detected only in coriander.
paprika and oregano. Gamma irradiation effectively sterilized all spice samples tested.
Warmbrod and Fry (48) evaluated the coliform and total
bacterial loads in spices, seasonings, and condiments as part
of a regulatory program conducted by the Food and Drug
Division of the state of Tennessee (U.S.) to determine if
those ingredients might be responsible for high bacterial
contents of sausages and other prepared meats. Spice
samples were collected from meat packing plants in Tennessee and then grouped as peppers (group I), prepared
sausage seasonings (group IlL frankfurter, bologna and
prepared meat seasonings (group III), and sage (Group IV).
Peppers were found to have the highest aerobic plate counts,
ranging from 3.0 103 to 2.8 107/g. Although sage had
the lowest overall aerobic plate count (<3.0 103 to 2.4
104/g), it also was reported to have the highest average
coliform count of any group (1.5 104/g). The authors
recommended a further study to compare microbial contamination of spices, seasonings, and condiments packed in
bulk with those packed in single, batch-size containers.
Yesair and Williams (49) reported on an investigation
conducted by the National Canners Association as part of a
study done in the U.S. on contamination of ingredients used
in canning. Forty types of spices and herbs were collected
from one spice manufacturer, four canners, and three meat
packers in the U.S. As with many studies, black pepper was
found to be the most heavily contaminated, with total counts
ranging from 1.2 106 to 1.6 x 107CFU/g. Black pepper
also contained the greatest quantities of acid-tolerant bacteria, total sporeformers, gas-forming spores, and aerobic
sporeformers. Overall, cloves (both whole and ground) were
found to be the least contaminated of the spices tested. The
authors concluded that there was a need for treatment to
reduce the bacterial content of spices.
nidulans.
A second study conducted in Spain by Garrido et a/. (56)
investigated the mold contamination and presence of ariatoxin-producing strains of Aspergil/us flavus in spices and
herbs purchased from supermarkets in Spain. Mold counts
were classified as very little (102 propagules/g) in ground
clove, ground cumin seed, ground tarragon, and nutmeg to
extremely high (105 propagules/g) in stick and ground
cinnamons, capers, saffron, badian, cardamom, juniper,
fennel, artemisia, bay leaf, mint, parsley, rock tea, and
ground mustard. Aspergillus spp. predominated in most
spices, although Penicil/ium spp. were the most common
mold genera in stick and ground cinnamons, turmeric, and
ground nutmeg. Four of the 13 strains of A. flavus examined
were found to fluoresce when grown on aflatoxin production
media.
Hashmi and Ghaffar (57), working in Karachi, Pakistan,
isolated 14 genera and 24 spp. of fungi from 88 samples of
coriander seeds from 15 countries. Samples from Pakistan
and India contained predominantly Alternaria alternata and
Fusarium moni/iforme. Other isolated fungi included Alternaria Iongissima, Boo3~tis cinerea, Fusarium equiseti, Protomyces macrosporus, and Pythium spinosum. Unlike other
studies, Aspergil/us and Penici//ium spp. were rarely detected except in heavily contaminated samples.
In another study done in Pakistan, Hashmi and Thrane (58)
studied the mycotoxins produced by species of Fusarium
isolated from capsicum, coriander, and fenugreek seeds.
Fusarium was isolated from 222 samples of capsicum, 88
samples of coriander, and 23 samples of fenugreek using
standard blotter techniques. A total of 1004 isolates representing six spp.--F, moniliforme, F. subglutinans, F. semitectum, F. solani, F. equiseti, and F. oxysporum--were
detected. A variety of mycotoxins were produced by the
isolated species.
Aspergil/us spp. were the most common molds detected in
10 samples of spices obtained from Japanese companies by
Juri et al. (17) in a study done in Japan. Unirradiated spices
had mold counts ranging from 1 x 102 to 2 x 104/g. Two
strains identified as A. flavus var. columnaris produced
aflatoxins. Ground black pepper stored in polyethylene
pouches at 35 C and 95% relative humidity supported rapid
mold growth during the first month of storage. An irradiation dose of 0.2 Mrad delayed mold growth in the ground
pepper, but was insufficient to suppress mold growth in
whole peppercorns. Unirradiated ground turmeric, ground
rosemary, whole rosemary, ground white pepper, and whole
white pepper also supported mold growth during storage,
with counts reaching a maximum of 106/g. An irradiation
dose of 0.4 Mrad was sufficient to eliminate mold growth in
all samples.
The growth of and aflatoxin production by Aspergillus
parasiticus (NRRL 2999) on natural and autoclaved cumin
and anise was studied by Llewellyn et al. (59) in Washington, D.C. Anise seeds and ground cumin were obtained
from a company in Virginia, while cumin seeds were
procured from a company in New Jersey, U.S.A. Country of
origin of the spices was not identified. Anise was reported to
be a better substrate for A. parasiticus than cumin, but both
anise and cumin seeds were found to support mycelial
growth, sporulation, and toxin production at room temperature if moisture was present in the samples. Aflatoxin
levels ranged from 0.83 to 6.5 ~g/g total for B 1, B 2, G I, and
G 2 in anise substrates. Only B l and G 1 were detected in
cumin samples at levels ranging from 0.23 to 0.63 p.g/g.
Marashetty (60) studied aflatoxins and aspergillus contamination in Indian spices in work done in Canada. A rapid
method developed for the study was able to detect aflatoxin
B 1 in black pepper, red pepper, ginger, and turmeric
samples destined for export from India at levels of 15 to
120 p.g/g. The most common species found in the spices
during drying were in the Aspergillus flavus-orvzae group.
Aspergillus-loaded pods, insect infestation, and high relative humidity were associated with mold contamination of
red pepper warehoused in Karnataka, India.
In another Spanish study, Martinez et al. (61) evaluated the
aflatoxin-producing ability of 35 of the Aspergillus flavus
strains isolated from the spices used by Garrido et al. (55).
Aflatoxins B 1, B2, GI, and G 2 were isolated from strains of
A. flavus found in white pepper, black pepper, and cayenne
pepper. A. flavus isolated from mustard powder, mint, and
mugwort produced only B l and B2. The authors concluded
that a health risk could be associated with the spices if they
were to be used in foods with appropriate conditions for
growth of and aflatoxin production by the molds.
Martinez-Magana et al. (62), working in Spain, studied the
mycoflora and Aspergillusflavus contamination of Spanish
pepper. Fifty-four samples representing 16 commercial
brands of whole and ground black and white pepper, green
pepper, and cayenne pepper on sale in Spain were evaluated. Average contamination was reported to be in the
103-104 propagules/g range for all samples, with the highest counts in white pepper and the lowest in green pepper.
The major mycofiora were Aspergillus and Penicillium spp.,
with A. flavus and A. glaucus most commonly isolated.
Twenty percent of the A. flavus isolates were reported to be
aflatoxigenic.
Enzyme-linked immunosorbent assay (ELISA) was used by
Notermans et al. (63) in The Netherlands to detect mold in a
variety of foods including spices. Samples of foods collected from commercial stores over a 3-y period were first
tested for the presence of aflatoxin B 1. Those found to
contain the aflatoxin were then tested for mold antigens
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of cumin seeds and chilli powder sold in retail shops in the city
of Bombay. Journal of Food Protection, 50, 418-419
(1987)
DE BOER, E. AND BOOT, E. M. Comparison of methods for
isolation and confirmation of Clostridium perfringens from
spices and herbs. Journal of Food Protection, 46, 533-536
(1983)
DE BOER, E., SPIEGELENBERG, W. M. AND JANSSEN, F. W.
Microbiology of spices and herbs. Antonie van Leeuwenhoek,
51, 435-438 (1985)
CASTELL,C. H. Thermophilic bacteria in foods and in various
ingredients entering into the manufacture of foods. Food
Research, 9, 410-414 (1944)
CHRISTENSEN,C. M., FANSE, H. A., NELSON, G. H., BATES,
F. AND MIROCHA, C. J. Microflora of black and red pepper.
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Summary
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Spices can contribute a significant number of microorganisms to food products. Although black pepper has often
been reported to contain the highest microbial loads, all
spices and herbs are susceptible to microbial contamination.
Growing conditions, harvesting and processing methods,
storage conditions, and post-harvest treatments should be
carefully controlled to prevent potential food spoilage and
food-borne illnesses due to contaminated spices and herbs.
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References
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40
41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60
61
62
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63
64
65
66
67
68
69
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