Food Protection Trends - January/February 2015 - 53

TABLE 3. Antibiotic resistance patterns of coliform species isolated from raw and RTE
broiler products
Coliform species

Resistance patterns

Enterobacter cloacae

Cip-Ap-Ts-E; Ap-Ts-E; Mem-Ap-Ts; Ap-E

Enterobacter sakazakii

Cip-Ts-E

Enterobacter aerogenes

Gm-Ak-Ap-Ts-E

Enterobacter amnigenus 2

Ap-E

Serratia liquefaciens

Ap-Ts-E; Ap-E

Klebsiella pneumoniae

Ctx-Mem-Ap-Ts-E; Ap-Ts-E; Ap-E

Klebsiella ozonae

E

Klebsiella ornitholytica

Ap-E

Hafnia alvei

Ap-Ts-E; Ap-E

Citrobacter freundii

Ap-E

Citrobacter braakii

Ap-E

Stenotrophomonas maltophilia

Cip-Mem-Ctx-Gm-Ak-Ap-E

Escherichia coli

Gm-E; Ap-E

Yersinia pseudotuberculosis

Ctx-Mem-Gm-Ak-Ap-Ts-E

Proteus mirabilis

Ap-Ts-E

Cip = ciprofloxacin; Ctx = cefotaxime; Mem = meropenem; Gm = gentamycin; Ak = amikacin; Ap = ampicillin;
TS = trimethoprim-sulphamethoxasole; E = erythromycin

study is lower than the incidence of 42% and 75% reported
for similar products in Korea and Taiwan, respectively
(4, 9). Similarly, the incidence of Stenotrophomonas
maltophilia (6.7%) in the current study is lower than the
78% reported by Qureshi et al. (27) in RTE salads in
the United Kingdom. Stenotrophomonas maltophilia has
been incriminated in cases of meningitis and pacemaker
endocarditis (30).
Multiple antibiotic resistance was noted among
coliforms isolated in the current study. Members of the
Enterobacteriaeceae family are commonly associated with
production of extended spectrum β-lactamases (ESBLs),
which enables their resistance to β-lactam antibiotics (7,
13). This attribute may be responsible for the observations
of the current study. Multiple antibiotic resistance was
similarly reported in large proportions of Klebsiella species
and E. coli isolated from slaughtered chickens in Italy
(37). Furthermore, Stenotrophomonas maltophilia was

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tract infections, was reported as an enteroinvasive pathogen
in 1998 (31). Yersinia pseudotuberculosis has also been
identified as a cause of gastroenteritis and lymphadenitis
in humans, with a fairly high case fatality rate (23) in the
United States. Enterobacter species are important nosocomial
pathogens, and are capable of causing various communityacquired infections (17). Although the pathogenic roles of
Serratia and Hafnia species are yet to be defined, they are
opportunistic pathogens that have also been incriminated in
nosocomial infections (14, 28). Therefore, the observations
in this study are of serious public health significance.
This finding is important, given that when undercooked
contaminated products are consumed, immunocompromised
persons are the most often affected, usually with high fatality
rates (6). In addition to the public health significance, Proteus
and Yersinia are generally associated with spoilage of meat
products (21), leading to product waste. In the case of RTE
products, the recovery rate of coliforms observed in this

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