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Journal of Food Safety ISSN 1745-4565

DETERMINATION OF ANTIBIOTIC RESISTANCE AND BIOGENIC

AMINE PRODUCTION OF LACTIC ACID BACTERIA ISOLATED
FROM FERMENTED TURKISH SAUSAGE (SUCUK)
ZGE YCEER and BANU ZDEN TUNCER1
Faculty of Engineering, Department of Food Engineering, Sleyman Demirel University, Isparta 32260, Turkey

Corresponding author.
TEL: +90-246-2111734;
FAX: +90-246-2370437;
EMAIL: banutuncer@sdu.edu.tr
Received for Publication July 2, 2014
Accepted for Publication November 29, 2014
doi: 10.1111/jfs.12177

ABSTRACT
The aim of this study was to isolate lactic acid bacteria (LAB) from sucuk and to
determine their antibiotic resistance and biogenic amine production abilities. A
total of 65 presumptive LAB were isolated and they were molecularly identified as
Pediococcus acidilactici (47.7%), Enterococcus faecium (36.9%), Lactobacillus sakei
ssp. carnosus (4.6%), Lactobacillus sakei ssp. sakei (4.6%), Pediococcus pentosaceus
(3.1%), Enterococcus faecalis (1.5%) and Weissella viridescens (1.5%) by sequencing 16S rDNA. The LAB were found resistant to clinically relevant antibiotics to
cure infections. Sixty-eight percent of the Enterococcus strains and the other entire
LAB displayed resistance from 2 to 8 of the antibiotics tested. All LAB did not
decarboxylate histidine, lysine or ornithine. The decarboxylase genes (hdc, ldc and
odc) were not detected in LAB. However, 68.0% of the Enterococcus strains decarboxylated tyrosine. The tyrosine decarboxylase gene (tdc) was also detected in
these tyraminogenic strains.

PRACTICAL APPLICATIONS
Lactic acid bacteria (LAB) are one of the most important groups of bacteria that
are known to be technologically important in the production of dry-fermented
sausages such as sucuk. The present study describes isolation, identification of
LAB from sucuk and determines their antibiotic resistance and biogenic amine
production abilities. LAB isolated from sucuk samples were found resistant to
clinically important antibiotics and most of them have multiple antibiotic resistance patterns. The findings of our study suggest that LAB in sucuk may play a
role to spread the antibiotic resistance between other bacteria including pathogens. In addition, most of the Enterococcus strains isolated from sucuk produce
tyramine. For these reasons, LAB isolated from sucuk may have a potential risk to
consumer health indirectly.

INTRODUCTION
Traditional fermented meat products have been produced
for many years and sucuk is one of them, which is most
popular in Turkey and in many Middle Eastern, Middle
Asian and Southern European countries (Stajic et al. 2013).
Sucuk is made of minced beef meat and/or water buffalo
and fatty tissue. Salt is the main additive, and besides this,
nitrite or nitrate is used for antibacterial, antioxidant and
color curative and different spices are also used. Sugar as a
source of carbohydrate is added to the mix to be utilized by
276

lactic acid bacteria (LAB) during fermentation. The prepared mix is filled into the air-dried bovine small intestine
and then the product is allowed to ferment and ripened
under controlled conditions for a certain period (Kaban
2013).
The microflora of dry-fermented sausage involves mainly
LAB, coagulase-negative Staphylococci and Kocuria species
and less importantly yeasts and molds (Ruiz-Moyano et al.
2009). It is reported that the dominant species for Turkish
dry-fermented sucuk is Lactobacillus plantarum (Kaban and
Kaya 2008; Adiguzel and Atasever 2009). On the contrary,
Journal of Food Safety 35 (2015) 276285 2015 Wiley Periodicals, Inc.

. YCEER and B. ZDEN TUNCER

various LAB counts were mentioned by different researchers. They have isolated Lactobacillus sakei, Lactobacillus
fermentum, Lactobacillus brevis, Lactobacillus rhamnosus,
Lactobacillus delbrueckii, Lactococcus lactis ssp. lactis,
Pediococcus pentosaceus, Pediococcus acidilactici, Leuconostoc
mesenteroides/dextranicum, Leuconostoc lactis, Enterococcus
faecium and Enterococcus faecalis species from sucuk
(Grakan et al. 1995; zdemir 1999; Con and Gkalp 2000;
Kaban and Kaya 2008; Adiguzel and Atasever 2009;
zmen-Togay et al. 2010). LAB metabolized carbohydrates,
lipids and nitrogenous compounds in sucuk and gain to
provide sausages unique color, taste and odor. They are
useful in meat fermentation process with their metabolites
and they can also improve sensory properties of dryfermented sausage with the production of small amounts of
acetic acid, ethanol, acetoin, pyruvic acid and carbon
dioxide. LAB also produce lactic acid by fermenting sugars
and thus unfavorable conditions for pathogenic and spoilage bacteria occur, and in this way, they play an influential
role in improving the shelf life and product safety (Krckel
2013).
LAB are usually considered as GRAS (Generally Recognize As Safe), safe bacteria. However, a few of the problems encountered in LAB are the potential to contain
antibiotic resistance and having the ability to produce biogenic amines (BAs). Antibiotic resistance of LAB could be
intrinsic or acquired. Antibiotic resistance genes in LAB
are often located on transferable plasmids or transposons;
therefore, these bacteria may create a repository of antibiotic resistance genes. Although LAB are not pathogenic
itself, they can transfer their antibiotic resistance genes to
pathogenic bacteria and thus cause health problems in
humans and animals (Mathur and Singh 2005; Toomey
et al. 2010; Gueimonde et al. 2013). It was reported that
LAB isolated from fermented meat products are mostly
resistant to kanamycin, tetracycline, penicillin, erythromycin and chloramphenicol (Hummel et al. 2007; Toomey
et al. 2010).
BAs have been regarded as natural toxic compounds and
can be a health risk after consumption of large amounts.
They can occur in a variety of foods, such as fish, meat,
cheese, vegetables and wines in high concentrations. BA
production is mainly related to the decarboxylation ability
of bacteria, and in the meat fermentation process, favorable
conditions may occur for BA production (such as microbial
growth, acidification and proteolysis) (Bover Cid et al. 2001;
Suzzi and Gardini 2003; de las Rivas et al. 2008). Histamine,
tyramine, putrescine and cadaverine are mainly consist of
BAs in foods. Several genera among LAB may produce BA
by decarboxylation of amino acids, e.g., Lactobacillus,
Carnobacterium, Pediococcus, Lactococcus, Enterococcus and
Leuconostoc (Silla-Santos 1996; Suzzi and Gardini 2003;
Komprda et al. 2010; Inoglu and Tuncer 2013).
Journal of Food Safety 35 (2015) 276285 2015 Wiley Periodicals, Inc.

ANTIBIOTIC RESISTANCE OF LACTIC ACID BACTERIA

Until today, there are not enough data about antibiotic

resistance and BA production abilities of LAB isolated from
sucuk, a traditional Turkish fermented meat product. This
research is the first report about the antibiotic susceptibility
and amino acid decarboxylase potential (phenotypic
expression and detecting of specific genes) of LAB isolated
from sucuk. The aim of this study was to isolate and determine LAB from sucuk, and to evaluate antibiotic resistance
and BA production.

MATERIAL AND METHODS

Sucuk Samples
A total of 20 sucuk samples produced without starter
culture were obtained from different manufacturers randomly in summer and autumn of 2013 from Afyonkarahisar province located in the Aegean region of Turkey.
The samples were transported on ice in a container to the
laboratory.

Isolation of LAB
After arrival to the laboratory, the sucuk casings were aseptically removed. Twenty-five grams of the samples was cut with
sterile lancet and transferred into a sterile stainless steel container of Waring blender (8011 ES HGB2WTS3, Torrington,
CT). Then, 225 mL of sterile physiological water (0.85%
NaCl) was added and homogenized for 1.5 min. Serial
decimal dilutions of the homogenized samples were prepared
and spread onto de Man Rogosa Sharpe (MRS) agar (Lab M,
Ltd., Bury, Lancashire, U.K.) and M17 agar (Merck, Darmstadt, Germany) with 0.5% glucose (GM17), incubated at 37
and 30C, respectively. The colonies were randomly picked
from each countable MRS and GM17 medium and all isolates were subjected to Gram staining and catalase testing.
Gram-positive and catalase-negative isolates were selected for
further studies. Stock cultures into an appropriate medium
with 20% glycerol were stored at 20C.

DNA Extraction
Bacterial genomic DNAs from LAB strains were
extracted from 0.5 mL of overnight cultures using a method
previously described by Cancilla et al. (1992). DNA
precipitates were dissolved in 50 L of TrisEDTA
(ethylenediaminetetraacetic acid) buffer (pH 8.0).

Identification of LAB
All of the isolates were characterized genotypically by 16S
rDNA homology using polymerase chain reaction (PCR)
with the following universal primers: pA (forward) 5-AGA
277

ANTIBIOTIC RESISTANCE OF LACTIC ACID BACTERIA

GTT TGA TCC TGG CTC AG-3 and pE (reverse) 5-CCG

TCA ATT CCT TTG AGT TT-3 (Edwards et al. 1989). The
final volume of 50 L of the PCR mixture was prepared using
3 L of the bacterial DNA solution, 1 L of each primer,
20 L nuclease-free water and 25 L of PCR master mix
(Fermentas, Vilnius, Lithuania). PCR for 16S rDNA gene was
performed in a programmable DNA thermocycler (Techne
TC3000, Cambridge, U.K.) using the following parameters:
initial denaturation step at 94C for 2 min, 30 amplification
cycles (denaturation at 94C for 30 s, annealing at 55C for 60 s
and elongation at 72C for 90 s) and a final extension step at
72C for 10 min. The amplicons were analyzed by electrophoresis on 1% (w/v) agarose gel (85 V for 1.5 h) in Trisacetate
EDTA buffer. After the electrophoresis, PCR products were
stained with ethidium bromide (20 g/mL) and visualized
under ultraviolet light. Gels were photographed using a
Nikon D5100 digital camera (Nikon Corp., Japan). The size
of amplicons was determined by comparison with
OGeneRuler 100-bp DNA ladder (Fermentas). Sequencing
of the 16S rDNA gene was performed in RefGen (ODT
Teknokent, Ankara, Turkey). Similarity search was conducted
using the BLAST software by NCBI (National Center for Biotechnology Information, Bethesda, MD).

. YCEER and B. ZDEN TUNCER

teicoplanin (30 g), linezolid (30 g) and levofloxacin

(5 g) (Oxoid Ltd., Basingstoke, U.K.). Antibiotic susceptibility of the Enterococcus strains and other LAB used in this
study was determined according to the recommendation of
Clinical and Laboratory Standards Institute (CLSI 2012)
and Charteris et al. (1998), respectively. E. faecalis ATCC
29212 was used as the control strain.

Biogenic Amine Production

BA production abilities of LAB were determined in the
decarboxylation medium described by Bover-Cid and
Holzapfel (1999). Pyridoxal-5-phosphate (at 0.005%) was
added to the medium as a cofactor for decarboxylation
reaction and the following precursor amino acids were also
added to the medium at 0.5% final concentration: histidine,
lysine, ornithine and tyrosine (Merck). Bromocresol purple
(Merck) was used as a color indicator and the medium was
autoclaved after pH was adjusted to 5.3. After 7 days of
aerobic incubation, BA production of the isolates was determined phenotypically by yellow to purple color changes in
the Petri dishes. Tyraminogenic E. faecium NYE54 strain
obtained from Inoglu and Tuncer (2013) was used as the
positive control.

Antibiotic Susceptibility Testing

For antibiotic susceptibility testing, a total of 1 mL of overnight LAB culture was centrifuged at 13,000 rpm
(15,493 g) for 5 min and washed twice with phosphate
buffered saline (PBS, pH 7.4). Pellets were resuspended in
2 mL of PBS to a turbidity of McFarland 0.5. Antibiotic susceptibility of strains was determined by disk diffusion
method onto MullerHinton agar medium against the following antibiotics: tetracycline (30 g), cephalothin (30 g),
chloramphenicol (30 g), clindamycin (2 g), cefoxitin
(30 g), ofloxacin (5 g), gentamicin (10 g), norfloxacin
(10 g), rifampicin (5 g), erythromycin (15 g), kanamycin (30 g), ampicillin (10 g), ciprofloxacin (5 g), penicillin (10 g), vancomycin (30 g), streptomycin (10 g or
300 g), doxycycline (30 g), minocycline (30 g), nitrofurantoin (300 g), quinupristin-dalfopristin (15 g),

Gene

Primer

Primer sequence (5 to 3)

hdc

HIS1-F
HIS1-R
CAD2-F
CAD2-R
PUT1-F
PUT1-R
TDC-F
TDC-R

GGNATNGTNWSNTAYGAYMGNGCNGA
ATNGCDATNGCNSWCCANACNCCRTA
GGDATNCCNGGNGGRTA
CAYRTNCCNGGNCAYAA
TWYMAYGCNGAYAARACNTAYTTYGT
ACRCANAGNACNCCNGGNGGRTANGG
TGGYTNGTNCCNCARACNAARCAYTA
ACRTARTCNACCATRTTRAARTCNGG

ldc
odc
tdc

Screening of Amino Acid

Decarboxylase Genes
Isolated genomic DNAs from LAB strains were subjected to
PCR amplification based on the method of de las Rivas et al.
(2006) in order to detect the presence of the following
decarboxylase genes: histidine (hdc), lysine (ldc), ornithine
(odc) and tyrosine (tdc). Primers used in this study were
given in Table 1. PCR for hdc, ldc, odc and tdc genes was performed using the following parameters: initial denaturation
step at 95C for 10 min, 30 amplification cycles (denaturation at 95C for 30 s, annealing at 53C for 30 s and elongation at 72C for 2 min) and a final extension step at 72C for
20 min. The amplification products were analyzed on 1.5%
(w/v) agarose gels. E. faecium NYE54 strain (tdc+) was used
as the positive control.

Fragment size (bp)

372

TABLE 1. PRIMERS AND FRAGMENT SIZES

FOR DETECTION OF AMINO ACID
DECARBOXYLASE GENES

1,185
1,440
825

Y: C or T; R: A or G; W: A or T; S: C or G; M: A or C; D: A, G or T.

278

Journal of Food Safety 35 (2015) 276285 2015 Wiley Periodicals, Inc.

. YCEER and B. ZDEN TUNCER

ANTIBIOTIC RESISTANCE OF LACTIC ACID BACTERIA

18 and 16 clinically important antibiotics for Enterococcus

and other LAB, according to the recommendation of Clinical and Laboratory Institute (CLSI 2012) and Charteris
et al. (1998), respectively. Antibiotic susceptibilities of the
strains were shown as R (resistance), I (intermediary) and S
(susceptible) in Tables 2 and 3. All Enterococcus strains were
found 100% sensitive to ampicillin, chloramphenicol, doxycycline, gentamicin, quinupristin-dalfopristin, minocycline,
streptomycin, teicoplanin, tetracycline and vancomycin. On
the contrary, Enterococcus strains were found most resistant
to rifampicin (72.0%), ciprofloxacin (52.0%) and nitrofurantoin (44.0%), followed by norfloxacin (16.0%), penicillin (12.0%) and erythromycin (4.0%) (Table 4). Most of the
Enterococcus strains (68.0%) showed multiple antibiotic
resistance patterns. The results of this study showed that
these strains displayed resistance from two to five of the
antibiotics tested.
All Pediococcus and Lactobacillus strains were found
completely (100%) sensitive to ampicillin, cephalothin,
chloramphenicol, clindamycin, erythromycin, rifampicin
and tetracycline. On the contrary, Pediococcus strains were

RESULTS
Isolation and Identification of LAB
A total of 65 gram-positive and catalase-negative presumptive LAB strains were isolated on MRS and GM17 agar
plates from 20 sucuk samples produced without a starter
culture. Presumptive LAB strains were identified genotypically by 16S rDNA homology. Sequence similarity of an
approximately 900 base pair (bp) PCR amplification products were determined by BLAST program and compared to
GenBank. Species were identified as 31 Pediococcus
acidilactici (47.7%), 24 E. faecium (36.9%), 3 Lb. sakei ssp.
carnosus (4.6%), 3 Lb. sakei ssp. sakei (4.6%), 2 Pediococcus
pentosaceus (3.1%), 1 E. faecalis (1.5%) and 1 Weissella
viridescens (1.5%).

Antibiotic Susceptibility Testing

Antibiotic susceptibility of strains was determined by disk
diffusion method onto MullerHinton agar medium against

TABLE 2. ANTIBIOTIC SUSCEPTIBILITY OF ENTEROCOCCUS STRAINS ISOLATED FROM SUCUK

Antibiotics
Strain

DO

NOR

VA

RD

MH

LEV

CIP

AMP

QD

TE

CN

LZD

TEC

E. faecium OBS 3
E. faecium OBS 4
E. faecium OBS 11
E. faecium OBS 12
E. faecium OBS 13
E. faecium OBS 14
E. faecium OBS 15
E. faecalis OBS 18
E. faecium OBS 20
E. faecium OBS 23
E. faecium OBS 24
E. faecium OBS 25
E. faecium OBS 26
E. faecium OBS 29
E. faecium OBS 31
E. faecium OBS 32
E. faecium OBS 33
E. faecium OBS 34
E. faecium OBS 37
E. faecium OBS 39
E. faecium OBS 41
E. faecium OBS 45
E. faecium OBS 46
E. faecium OBS 47
E. faecium OBS 48

S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S

I
S
S
R
R
S
I
I
I
S
I
R
R
I
I
I
I
I
I
I
I
I
S
I
I

S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S

S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S

R
S
S
S
S
S
S
R
R
S
R
R
R
R
R
R
R
R
R
R
R
R
R
R
R

S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S

S
S
S
S
S
S
S
S
S
S
S
S
R
R
R
S
S
S
S
S
S
S
S
S
S

S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S

I
S
S
S
S
S
I
I
I
S
I
S
I
I
I
S
I
S
I
S
S
I
I
S
S

R
S
I
S
I
I
I
R
R
S
I
R
R
R
R
I
R
I
R
R
I
R
I
R
R

S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S

S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S

R
S
S
S
S
I
S
R
R
R
R
R
R
R
R
R
I
R
I
I
S
I
S
I
I

S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S

S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S

I
S
I
R
I
S
I
I
I
I
I
I
I
I
I
I
I
I
I
I
I
I
I
I
I

S
S
S
S
S
S
S
I
I
S
S
I
S
I
S
S
S
S
S
S
S
S
S
S
S

S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S

Susceptibilities of Enterococcus strains were determined according to CLSI (2012).

DO, doxycycline (30 g); NOR, norfloxacin (10 g); VA, vancomycin (30 g); C, chloramphenicol (30 g); RD, rifampicin (5 g); MH, minocycline
(30 g); P, penicillin (10 g); S, streptomycin (300 g); LEV, levofloxacin (5 g); CIP, ciprofloxacin (5 g); AMP, ampicillin (10 g); QD, quinupristindalfopristin (15 g); F, nitrofurantoin (300 g); TE, tetracycline (30 g); CN, gentamicin (120 g); E, erythromycin (15 g); LZD, linezolid (30 g); TEC,
teicoplanin (30 g).
I, intermediary; S, susceptible; R, resistance.

Journal of Food Safety 35 (2015) 276285 2015 Wiley Periodicals, Inc.

279

ANTIBIOTIC RESISTANCE OF LACTIC ACID BACTERIA

. YCEER and B. ZDEN TUNCER

TABLE 3. ANTIBIOTIC SUSCEPTIBILITY OF LACTOBACILLUS, PEDIOCOCCUS AND WEISSELLA STRAINS ISOLATED FROM SUCUK
Antibiotics
Strain

TE

KF

DA

FOX

OFX

CN

NOR

RD

AMP

CIP

VA

Lb. sakei ssp. carnosus OBS 1

P. acidilactici OBS 2
Lb. sakei subsp. carnosus OBS 5
P. acidilactici OBS 6
P. acidilactici OBS 7
Lb. sakei ssp. sakei OBS 8
Lb. sakei ssp. sakei OBS 9
P. acidilactici OBS 10
P. acidilactici OBS 16
Lb. sakei ssp. sakei OBS 17
P. acidilactici OBS 19
P. acidilactici OBS 21
P. acidilactici OBS 22
P. acidilactici OBS 27
P. acidilactici OBS 28
P. acidilactici OBS 30
P. acidilactici OBS 35
P. acidilactici OBS 36
P. acidilactici OBS 38
P. acidilactici OBS 40
P. acidilactici OBS 42
W. viridescens OBS 43
P. acidilactici OBS 44
P. acidilactici OBS 49
Lb. sakei subsp. carnosus OBS 50
P. acidilactici OBS 51
P. acidilactici OBS 52
P. acidilactici OBS 53
P. acidilactici OBS 54
P. acidilactici OBS 55
P. pentosaceus OBS 56
P. pentosaceus OBS 57
P. acidilactici OBS 58
P. acidilactici OBS 59
P. acidilactici OBS 60
P. acidilactici OBS 61
P. acidilactici OBS 62
P. acidilactici OBS 63
P. acidilactici OBS 64
P. acidilactici OBS 65

S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
R
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S

S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
I
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S

S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S

S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
R
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S

I
R
R
R
R
S
S
I
I
I
R
R
R
R
R
R
R
R
R
R
R
R
R
R
I
I
R
R
R
R
R
R
R
R
R
R
R
R
R
R

R
R
R
R
R
R
R
R
R
R
R
R
R
R
R
R
R
R
R
R
R
I
R
R
R
R
R
R
R
R
R
R
R
R
R
R
R
R
R
R

R
R
R
R
S
S
S
R
R
S
S
S
R
R
R
R
R
R
R
R
R
R
R
S
S
R
R
R
R
R
R
R
S
R
S
R
R
R
R
S

I
R
R
R
R
R
R
R
I
R
R
R
R
R
R
R
R
R
R
R
R
I
R
R
R
R
R
R
R
R
R
R
R
R
R
R
R
R
R
R

S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S

S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S

R
R
I
R
R
I
I
R
R
I
R
R
R
R
R
R
R
R
R
R
R
R
R
R
S
R
R
R
R
R
R
R
R
R
R
R
R
R
R
R

S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S

S
R
R
R
R
R
R
R
I
R
R
R
R
R
R
R
R
R
R
R
R
I
R
R
R
R
R
R
R
R
R
R
I
R
R
R
R
R
R
R

S
S
S
S
S
S
S
S
I
S
S
S
S
S
S
S
S
S
S
S
S
R
S
S
S
S
S
S
S
S
S
S
R
S
S
S
S
S
S
S

S
R
R
R
R
R
R
R
S
R
R
R
R
R
R
R
R
R
R
R
R
S
R
R
R
R
R
R
R
R
R
R
S
R
R
R
R
R
R
R

R
R
R
R
R
R
R
R
R
R
R
R
R
R
R
R
R
R
R
R
R
R
R
R
I
R
R
R
R
R
R
R
R
R
R
R
R
R
R
R

Susceptibilities of Lactobacillus, Pediococcus and Weissella strains were determined according to Charteris et al. (1998).
TE, tetracycline (30 g); KF, cephalothin (30 g); C, chloramphenicol (30 g); DA, clindamycin (2 g); FOX, cefoxitin (30 g); OFX, ofloxacin (5 g);
CN, gentamicin (10 g); NOR, norfloxacin (10 g); RD, rifampicin (5 g); E, erythromycin (15 g); K, kanamycin (30 g); AMP, ampicillin (10 g); CIP,
ciprofloxacin (5 g); P, penicillin (10 g); VA, vancomycin (30 g); S, streptomycin (10 g).
I, intermediary; S, susceptible; R, resistance.

found completely resistant to kanamycin, ofloxacin and

streptomycin. In addition, Pediococcus strains exhibited
resistance to norfloxacin (96.97%), ciprofloxacin (93.94%),
vancomycin (93.9%), cefoxitin (90.9%) and gentamicin
(78.79%). The Lactobacillus strains were found only 100%
resistant to ofloxacin. However, these strains were shown to
be the most resistant to ciprofloxacin (83.33%), norfloxacin
280

(83.33%), streptomycin (83.33%) and vancomycin

(83.33%), followed by gentamicin (33.33%), cefoxitin
(16.67%) and kanamycin (16.67%) (Table 4). All
Pediococcus and Lactobacillus strains showed multiple antibiotic resistance patterns. Pediococcus and Lactobacillus
strains displayed resistance from four to eight and four to
seven of the antibiotics tested, respectively.
Journal of Food Safety 35 (2015) 276285 2015 Wiley Periodicals, Inc.

. YCEER and B. ZDEN TUNCER

ANTIBIOTIC RESISTANCE OF LACTIC ACID BACTERIA

TABLE 4. ANTIBIOTIC SUSCEPTIBILITY AND RESISTANCE (%) OF LAB STRAINS ISOLATED FROM SUCUK
Pediococcus (n = 33)

Enterococcus (n = 25)

Lactobacillus (n = 6)

Antibiotic

Concentration
(g/disk)

Weissella viridescens (n = 1)

S (%)

I (%)

R (%)

S (%)

I (%)

R (%)

S (%)

I (%)

R (%)

S (%)

I (%)

R (%)

TE
KF
C
DA
FOX
OFX
CN
NOR
RD
E
K
AMP
CIP
P
VA
S
DO
MH
S
LEV
QD
F
LZD
TEC

30
30
30
2
30
5
10
10
5
15
30
10
5
10*
30
10
30
30
300
5
15
300
30
30

100
100
100
100
0
0
21.21
0
100
100
0
100
0
93.94
6.06
0
NT
NT
NT
NT
NT
NT
NT
NT

0
0
0
0
9.09
0
0
3.03
0
0
0
0
6.06
3.03
0
0
NT
NT
NT
NT
NT
NT
NT
NT

0
0
0
0
90.91
100
78.79
96.97
0
0
100
0
93.94
3.03
93.94
100
NT
NT
NT
NT
NT
NT
NT
NT

100
NT
100
NT
NT
NT
100
20
28
8
NT
100
12
88
100
NT
100
100
100
52
100
28
84
100

0
NT
0
NT
NT
NT
0
64
0
88
NT
0
36
0
0
NT
0
0
0
48
0
28
16
0

0
NT
0
NT
NT
NT
0
16
72
4
NT
0
52
12
0
NT
0
0
0
0
0
44
0
0

100
100
100
100
33.33
0
66.67
0
100
100
16.67
100
16.67
100
16.67
0
NT
NT
NT
NT
NT
NT
NT
NT

0
0
0
0
50
0
0
16.67
0
0
66.66
0
0
0
0
16.67
NT
NT
NT
NT
NT
NT
NT
NT

0
0
0
0
16.67
100
33.33
83.33
0
0
16.67
0
83.3
0
83.33
83.33
NT
NT
NT
NT
NT
NT
NT
NT

0
0
100
0
0
0
0
0
100
100
0
100
0
0
100
0
NT
NT
NT
NT
NT
NT
NT
NT

0
100
0
0
0
100
0
100
0
0
0
0
100
0
0
0
NT
NT
NT
NT
NT
NT
NT
NT

100
0
0
100
100
0
100
0
0
0
100
0
0
100
0
100
NT
NT
NT
NT
NT
NT
NT
NT

* Penicillin G 10 U/disk.
TE, tetracycline; KF, cephalothin; C, chloramphenicol; DA, clindamycin; FOX, cefoxitin; OFX, ofloxacin; CN, gentamicin; NOR, norfloxacin; RD, rifampicin; E, erythromycin; K, kanamycin; AMP, ampicillin; CIP, ciprofloxacin; P, penicillin; VA, vancomycin; S, streptomycin; DO, doxycycline; MH,
minocycline; LEV, levofloxacin; QD, quinupristin-dalfopristin; F, nitrofurantoin; LZD, linezolid; TEC, teicoplanin; NT, not tested.
I, intermediary; S, susceptible; R, resistance.

W. viridescens OBS43 strain was found sensitive to ampicillin, chloramphenicol, erythromycin, rifampicin and vancomycin. The OBS43 strain was resistant to cefoxitin,
clindamycin, gentamicin, kanamycin, penicillin, streptomycin and tetracycline. In addition, this strain was intermediary resistant to cephalothin, ciprofloxacin, norfloxacin and
ofloxacin (Table 3).

Biogenic Amine Production

None of the LAB decarboxylated histidine, lysine and ornithine. On the contrary, 16 E. faecium and 1 E. faecalis strains
among LAB isolated in this study were able to decarboxylate
tyrosine on the decarboxylation medium.

Screening of Amino Acid

Decarboxylase Genes
Histidine, lysine and ornithine decarboxylase genes (hdc, ldc
and odc, respectively) were not detected in any LAB. Tyrosine decarboxylation gene (tdc) was detected in all
Journal of Food Safety 35 (2015) 276285 2015 Wiley Periodicals, Inc.

tyraminogenic Enterococcus strains (Fig. 1). All the

tyraminogenic strains amplified about 825 bp fragment
with the tdc gene primers as expected.

DISCUSSION
LAB play an important role in the production of dryfermented sausages. In sucuk batters, LAB counts vary
between 102 and 104 cfu/g. LAB demonstrate a significant
growth during fermentation and constitute the dominant
microflora (Kaban 2013). In the present study, the dominant species of LAB were determined as P. acidilactici
(47.7%) and subsequently E. faecium (36.9%). Conversely
to our results, most of the previous studies showed that Lactobacilli species, especially Lb. plantarum and Lb. sakei were
identified as a dominant microbiota in fermented sausage.
On the contrary, Lb. pentosus, Lb. curvatus, Lb. fermentum,
Lb. brevis, Lb. delbrueckii, Lb. rhamnosus, Lc. lactis ssp.
lactis, P. pentosaceus, P. acidilactici, Le. mesenteroides ssp.
mesenteroides/dextranicum and Le. lactis isolated from
sausage by different researchers (Kaban and Kaya 2008;
281

ANTIBIOTIC RESISTANCE OF LACTIC ACID BACTERIA

. YCEER and B. ZDEN TUNCER

FIG. 1. POLYMERASE CHAIN REACTION SCREEN FOR TYROSINE DECARBOXYLASE GENE FROM SOME ENTEROCOCCUS FAECIUM AND
PEDIOCOCCUS ACIDILACTICI STRAINS BY USING PRIMERS TDC-F AND TDC-R
Order lane 1, E. faecium OBS20; lane 2, P. acidilactici OBS21; lane 3, P. acidilactici OBS22; lane 4, E. faecium OBS23; lane 5, E. faecium OBS24; lane
6, E. faecium OBS25; lane 7, E. faecium OBS26; lane 8, P. acidilactici OBS27; lane 9, P. acidilactici OBS28; lane M, 100 bp DNA ladder (Fermentas);
lane 10, E. faecium OBS29; lane 11, P. acidilactici OBS30; lane 12, E. faecium OBS31; lane 13, E. faecium OBS32; lane 14, E. faecium OBS33; lane
15, E. faecium OBS34; lane 16, P. acidilactici OBS35; lane 17, P. acidilactici OBS36; lane 18, E. faecium NYE54 (positive control); lane 19, negative
control.

Adiguzel and Atasever 2009; Kaban 2013; Landeta et al.

2013). Our study is the first report that the dominant flora
of Turkish dry-fermented sausage was determined as
P. acidilactici and E. faecium. Besides this statement, some
other researchers reported that Enterococcus species can be
found in high prevalence in a spontaneously fermented
meat products produced in some European countries
similar to our results (Ruiz-Moyano et al. 2008; Marty et al.
2012; Landeta et al. 2013). Many sausage producers use
Pediococcus acidilactici as a starter culture, but in our study,
sausage samples were naturally fermented meat products.
Thus, our observations were drawn attention. Weissella
viridescens, Weissella halotolerans and Weissella hellenica
strains were usually known as spoilage microorganisms
associated with meat and meat products. It is indicated that
these strains significantly occur in low numbers in sausage
(Albano et al. 2009), as confirmed in this study.
Bacterial resistance to antibiotics is a worldwide problem
for both human and veterinary medicine. LAB are usually
consumed in high quantities and close contact with other
bacteria in the human gastrointestinal tract provides perfect
conditions for horizontal transfer of conjugative plasmids
and transposons with genes encoding resistance to antimicrobial agents (Dukov and Karpkov 2013). In this
study, Enterococcus strains isolated from sucuk were found
susceptible to many antibiotics used as drugs in human
infections such as vancomycin, chloramphenicol and ampicillin similar to some other research (Riboldi et al. 2009;
Toomey et al. 2010). However, contrary to our study, it is
often indicated that most of the Enterococcus originated
meat and meat products are resistant to ampicillin, streptomycin and tetracycline (Koluman et al. 2009; Valenzuela
et al. 2009). In addition, zmen-Togay et al. (2010)
282

reported that Enterococcus strains isolated from Turkish

sausage were resistant to chloramphenicol, tetracycline and
gentamicin. The reported studies suggested that antibiotic
resistance in Enterococcus from meat products varied. Susceptibility to clinically relevant antibiotics of enterococci of
food origin is very important for consumer health (zden
Tuncer et al. 2013). For this reason, the 100% susceptibility
to clinically important antibiotics such as ampicillin,
chloramphenicol, doxycycline, gentamicin, quinupristindalfopristin, minocycline, streptomycin, teicoplanin, tetracycline and vancomycin of Enterococcus strains isolated in
this study is advantageous. Most of the Lactobacilli were
known as sensitive to penicillin, chloramphenicol, kanamycin, tetracycline and gentamicin similar to our results, but
it is also reported that vancomycin, tetracycline and
rifampicin-resistant Lactobacilli were also isolated from drycured sausage (Zdolec et al. 2011; Patel et al. 2012; Landeta
et al. 2013). Similar results were obtained by different
researchers for Pediococcus isolated from home-made yogurt
and Turkish dry-fermented sausage (Beyatli et al. 2007;
Yuksekdag and Aslim 2010). Resistance to the glycopeptide
antibiotic vancomycin in Pediococcus and Lactobacillus
strains isolated from sucuk were remarkable due to the use
of vancomycin in many infections in humans. Liu et al.
(2009) reported that their fish originated W. viridescens isolates were resistant to gentamicin, streptomycin and kanamycin, as confirmed in this study. On the contrary, they
found these strains to be sensitive to tetracycline contrary to
our result.
Another undesirable ability of LAB in fermented food
products is their BA production properties. According to
our results, only 68% of Enterococcus strains isolated from
sucuk samples were decarboxylated tyrosine and other LAB
Journal of Food Safety 35 (2015) 276285 2015 Wiley Periodicals, Inc.

. YCEER and B. ZDEN TUNCER

were did not decarboxylate any of the amino acid precursors used in this study. Similar to our results, E. faecium and
E. faecalis isolated from sausage and cheeses were also identified as tyramine producers by different researchers
(Komprda et al. 2010; Inoglu and Tuncer 2013). Contrary to
our results, Lorencov et al. (2012) found that some Lactobacillus strains and one Pediococcus strain isolated from
dairy products produced tyramine, cadaverine and small
amount of putrescine. It has also been reported that tyramine producer E. faecium and Lb. sakei were isolated from
dry-cured sausage (Landeta et al. 2013). In our study, PCR
assays confirmed the results of decarboxylation medium. A
100% correlation between the results of conventional
culture methods and PCR assays has been demonstrated, as
reported by Inoglu and Tuncer (2013). BA concentration
can be high in fermented meat products based on the decarboxylating activity of bacteria and meat enzymes. Especially,
tyramine and histamine in high concentrations may affect
vulnerable individuals and they may have some health
problems such as migraine and hypertensive crisis
(Latorre-Moratalla et al. 2008). In addition, it has also been
reported that putrescine and cadaverine increase the toxicity
effects of tyramine and histamine. In addition to toxicological effects, during the heating of meat products, if there are
putrescine and cadaverine together with spermidine and
spermine, natural polyamines, or with nitrite/nitrate, may
lead to the formation of carcinogenic nitroso amines
(Drabik-Markiewicz et al. 2009; De Mey et al. 2014). For
these reasons, BA production in fermented foods is important for consumer health.
In conclusion, the results of this study indicated that LAB
isolated from sucuk samples were found resistant to clinically important antibiotics and most of them have multiple
antibiotic resistance patterns. The findings of our study
suggest that LAB in sucuk may play a role in spreading the
antibiotic resistance between other bacteria including
pathogens. In addition, most of the Enterococcus strains isolated from sucuk produce tyramine. For these reasons, LAB
isolated from natural fermented meat products such as
sucuk may have potential risk to consumer health indirectly.

ACKNOWLEDGMENT
This research was financially supported by Sleyman
Demirel University, Scientific Research Project Coordination Unit through Project No. 3818-YL2-13.
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