Prevalence and antibiotic resistance of Listeria species in meat
Department of Biology, Faculty of Science and Art, Gazi University, 06500 Teknikokullar, Ankara, Turkey
Received 2 July 2003; accepted 24 March 2004
In this study, a total of 146 raw (minced, chicken, beef) and cooked (red meat, chicken) meat samples were analysed for the
presence of Listeria spp. The isolates were characterized by morphological, cultural, biochemical tests according to Bergey’s manualand conﬁrmed by API-Listeria kit. Out of a total of 146 meat samples, 79 (54.10%) were found to be contaminated with Listeriaspp., with the highest incidence (86.4%) occurring in raw minced meat. Listeria monocytogenes was isolated from 9 (6.16%) of the 79samples examined. Other species isolated included L. innocua 68 (46.57%), L. welshimeri one (0.68%) and L. murrayi one (0.68%). Of the Listeria species, L. innocua (46.57%) was the most predominantly isolated species in a variety of meat samples. Overall, theListeria strains isolated from meat and meat products were mostly resistant to cephalothin and nalidixic acid but exhibited a highdegree of susceptibility to kanamycin, chloramphenicol and tetracycline. The importance of ﬁnding antibiotic resistant Listeria spp. in food is discussed. r 2004 Elsevier Ltd. All rights reserved.
Keywords: Listeria spp.; Meat samples; Antibiotic resistance
Listeria species are ubiquitous bacteria widely dis-
tributed in the natural environment. The ubiquitous
these foods have not been associated with documented
character of the bacteria inevitably results in contam-
outbreaks of human listeriosis. The detection of Listeria
ination of numerous food products. Epidemiological
spp. in meat is of particular concern in terms of
studies performed in recently years have demonstrated
consumer safety, as these organisms are capable of
that Listeria monocytogenes is an important pathogen
growing on both raw and cooked meat at refrigeration
Although dairy products have been major source
during further transformation processes of raw meat
into meat products L. monocytogenes can be introduced,
other raw or recontaminated products of animal
where the amount depends on the extent of cross-
or vegetable origin may serve as vehicles of transmission
contamination, personal and general hygienic measures
of this pathogen. To date, there have been almost no
reports of outbreaks of foodborne listeriosis associated
addition, assessing the prevalence of L. monocytogenes
with meat consumption. However, Listeria spp. has
in cooked meat is particularly important, since these
been isolated from poultry, red meat and meat products
products are often consumed after a brief heat
in many countries around the world such as Yugoslavia
treatment, which may not be sufﬁcient to kill all viablecells (
Despite efﬁcient antibiotic therapy, listeriosis repre-
*Corresponding author. Tel.: +90-312-212-60-30; fax: +90-312-
sents a public health problem since it is fatal in up to
E-mail address: firstname.lastname@example.org (N. Y .ucel).
30% of the cases. This threatening nature of listeriosis
0740-0020/$ - see front matter r 2004 Elsevier Ltd. All rights reserved. doi:10.1016/j.fm.2004.03.007
N. Y .ucel et al. / Food Microbiology 22 (2005) 241–245
Table 1Incidence of Listeria species from various meat products
a Parenthesis indicate percentage of positive samples.
also prompted the World Health Organization (WHO)
after 48 h of incubation at 37C. The suspect colonies
to suggest that various food products must be frequently
were subcultured to tryptone soy agar supplemented
investigated for the presence of L. monocytogenes on a
with 0.6% yeast extract (TSA-YE, LabM) for purity
and incubated at 37C. Every colony was conﬁrmed by
Although occurrence of Listeria species in meat and
biochemical reactions and morphology, including Gram
meat products has been investigated in several countries,
staining, catalase production, oxidase, motility and
little has been reported about the incidence of the
Voges Praskauer reaction. For further conﬁrmation of
organisms in meat products in Turkey. The purpose of
Listeria spp., other biochemical reactions, b-haemolytic
this study is to investigate the incidence of Listeria
activity, and the CAMP tests were performed according
species in raw and cooked meat products and to check
to Bergey’s Manual of Systematic Bacteriology
antibiotic resistance patterns of the isolated strains.
The isolates of L. monocytogenes andListeria spp. were identiﬁed using the API-Listeria(BioMerieux, Florence), along with the reference strains
L. monocytogenes ATCC 19114 and L. innocua ATCC33090.
The samples were collected from approximately 200 g
of meat obtained from the supermarkets, local butcher-
All the isolates of Listeria were tested by the standart
shops and restaurants located in Ankara from May 2001
to April 2002. The types and numbers samples collected
from each of the sources are shown in All
following antibiotics were spotted with a 3 cm interval
samples were stored at 4C after sampling, until the
ampicillin (10 mg), chloramphenicol (30 mg), cephalothin
(30 mg), ciproﬂoxacin (5 mg), kanamycin (30 mg), tri-methoprim/sulfamethoxazole (SXT) (1.25/23.75 mg), na-
2.2. Isolation and identification of Listeria species
lidixic acid (30 mg), tetracycline (30 mg), and tobramycin(10 mg). Isolates were cultured in trypticase-soy broth
Meat samples were analysed for the presence of
(TSB) supplemented with 0.6% yeast extract, and
Listeria spp. using the enrichment and isolation
transferred to Mueller–Hinton agar (Oxoid CM 337).
procedure, recommended by the USDA-FSIS Method
The plates were incubated at 37C for 48 h.
Twenty-ﬁve grams of a samplewas aseptically taken, blended for 2 min in 225 ml ofUVM (University of Vermont) Listeria enrichment
broth (UVM 1) (composition in g/l: tryptose 10; meatextract 5; yeast extract 5; NaCl 20; K2HPO4 1.35; esculin
presented the types, numbers and sources of
1; nalidixic acid 0.02; acriﬂavine hydrochloride 0.012;
the meat samples analysed in this study. Of a total of
pH: 7.2), and incubated at 37C for 24 h. A portion of
146 samples examined, 79 (54.1%) were positive for
1 ml of primary enrichments were transferred to 9 ml of
Listeria spp. The ﬁndings of our study are in agreement
UVM 2 (UVM 1 with 0.025 g/l of acriﬂavine hydro-
chloride in 10 ml of sterile distilled water, pH: 7.2) and
incubated at 37C for 24 h. Secondary enrichments
spp. in 56.6% of meat samples. Similarly, in a study in
(0.1 ml) were streaked to modiﬁed Oxford agar (Oxoid)
Switzerland, isolated the Listeria spp.
and plates were examined for typical Listeria colonies
from 55.3% of raw chicken samples. In this study all the
N. Y .ucel et al. / Food Microbiology 22 (2005) 241–245
Table 2Percentage and number of isolates of 79 Listeria resistant to 9 antimicrobial agents
various meat products, raw minced meat had the highest
incidence of Listeria spp., with 37 (86.4%) of 42 samples
According to these results, the existence of Listeria spp. in
being positive. Incidence of Listeria spp. in raw meats
meats would pose a threat only if the meat were
could be attributed either to fecal contamination during
insufﬁciently cooked or if there is cross-contamination. It
was signiﬁcantly important for public health to detect
According to previous some reports, high incidences of
Listeria spp., and particularly L. monocytogenes, in meat
L. monocytogenes were found in raw meat.
products sold in Ankara, since consumers are frequently
isolated L. monocytogenes in 69% of minced meat
exposed to these products. However, in Turkey raw meat
is normally thoroughly cooked or grilled before consump-
detected the bacteria in 24% of beef in Australia.
tion, and L. monocytogenes is likely to be eliminated.
isolated it in 34% of raw meat in Japan.
It is interesting to note that L. innocua was isolated
Some investigators have also found the incidence of L.
predominantly among Listeria species in our study
monocytogenes to be moderate: 12.5% in New Zealand
(). It was detected in 83.3% of the raw minced
meat, 57.6% of the raw chicken meat, 63.1% of the raw
beef, 9.6% of the cooked red meat and 10.7% of the
cooked chicken samples. This ﬁnding is in agreement
In the present study, we analysed raw meat samples
with other studies where L. innocua was the most
and the incidence of L. monocytogenes was found to be
common species in raw and cooked meats, while other
4.7% in minced meat, 11.5% in chicken and 5.2% in
beef. These results are in close agreement with the
Until recently, the Listeria genus was thought to be
, where the organism was recovered from 4.3%
uniformly susceptible to antibiotics active against
and 12.5% of meat samples, respectively. Also, in our
Gram-positive bacteria including ampicillin or penicillin
study, L. monocytogenes was isolated in cooked meat
(combined with aminoglycosides), trimethoprim (alone
products (red meat 3.5%, chicken meat 6.4%). The
or combined with sulfamethoxazole), tetracyclines,
incidence of L. monocytogenes in cooked meat was
erythromycin, and gentamicin. Hence, these antibiotics
similar to that reported by various authors: 7.9% in
were used treatment of human listeriosis and veterinary
ﬁrst antibiotic-resistant L. monocytogenes was described
5 to 21 samples of cook-chill food, and all isolations
resistant strains have been detected in food and sporadic
were from poultry dishes. The thermal resistance of
Listeria spp. and L. monocytogenes has been debated,
but it is generally accepted that proper heating kills
species is due to the acquisition of three type mobile
viable Listeria cells. However, the occurrence of Listeria
genetic elements: self-transferable and mobilizable plas-
spp. in cooked meats may be as considered a conse-
quence of inadequate heat treatment or post-heating
In our study, L. monocytogenes, L. innocua and L.
recontamination. On the other hand, L. monocytogenes
welshimeri were highly sensitive to chloramphenicol (88–
has been strongly implicated particularly in the con-
100%) and to tetracycline (100%, except L. seeligeri),
tamination of foods stored at low temperatures. Storage
but resistant to ampicillin (66–100%). Similarly,
of such products under such low temperature conditions
indicated that L. monocytogenes, L. innocua
may allow the growth of signiﬁcant numbers of these
isolated from meat products were high sensitivity to
organisms leading to foodborne illnesses among con-
N. Y .ucel et al. / Food Microbiology 22 (2005) 241–245
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