Characterization of integrons and resistance genes in multidrug-resistant
Salmonella enterica isolated from meat and dairy products in Egypt
Ashraf M. Ahmed
a
, Toshi Shimamoto
b
, Tadashi Shimamoto
b,
⁎
a
Department of Bacteriology, Mycology and Immunology, Faculty of Veterinary Medicine, Kafrelsheikh University, Kafr El-Sheikh 33516, Egypt
b
Laboratory of Food Microbiology and Hygiene, Graduate School of Biosphere Science, Hiroshima University, Higashi-Hiroshima 739-8528, Japan
abstract article info
Article history:
Received 28 February 2014
Received in revised form 22 July 2014
Accepted 23 July 2014
Available online 31 July 2014
Keywords:
β-lactamase
Enteritidis
Infantis
Plasmid-mediated
Typhimurium
Foodborne pathogens are a leading cause of illness and death, especially in developing countries. The problem is
exacerbated if bacteria attain multidrug resistance. Little is currently known about the extent of antibiotic resis-
tance in foodborne pathogens and the molecular mechanisms underlying this resistance in Africa. Therefore, the
current study was carried out to characterize, at the molecular level, the mechanism of multidrug resistance in
Salmonella enterica isolated from 1600 food samples (800 meat products and 800 dairy products) collected
from different street venders, butchers, retail markets and slaughterhouses in Egypt. Forty-seven out of 69 iso-
lates (68.1%) showed multidrug resistance phenotypes to at least three classes of antimicrobials. The incidence
of multidrug-resistant isolates was higher in meat products (37, 69.8%) than in dairy products (10, 62.5%). The
multidrug-resistant serovars included, S. enterica serovar Typhimurium (24 isolates, 34.8%), S. enterica serovar
Enteritidis, (15 isolates, 21.8%), S. enterica serovar Infantis (7 isolates, 10.1%) and S. enterica non-typable serovar
(1 isolate, 1.4%). The highest resistance was to ampicillin (95.7%), then to kanamycin (93.6%), spectinomycin
(93.6%), streptomycin (91.5%) and sulfamethoxazole/trimethoprim (91.5%). PCR and DNA sequencing were
used to screen and characterize integrons and antibiotic resistance genes and 39.1% and 8.7% of isolates were pos-
itive for class 1 and class 2 integrons, respectively. β-lactamase-encoding genes were identified in 75.4% of iso-
lates and plasmid-mediated quinolone resistance genes were identified in 27.5% of isolates. Finally, the
florphenicol resistance gene, floR, was identified in 18.8% of isolates. PCR screening identified S. enterica serovar
Typhimurium DT104 in both meat and dairy products. This is the first study to report many of these resistance
genes in dairy products. This study highlights the high incidence of multidrug-resistant S. enterica in meat and
dairy products in Egypt, with the possibility of their transfer to humans leading to therapeutic failure. Therefore,
the overuse of antibiotics in animals should be drastically reduced in developing countries.
© 2014 Elsevier B.V. All rights reserved.
1. Introduction
Increasing resistance to antimicrobial agents remains a major
challenge to public health professionals in both developed and develop-
ing countries. However, in developing countries, antimicrobial
resistance is exacerbated by over-prescription of antibiotics and
increased use in both human and animal healthcare. Furthermore, strat-
egies to combat and prevent resistance are not at the top of the list of
priorities in these countries (da Costa et al., 2013). More recently, the
Centers for Disease Control and Prevention of the USA estimates that,
in the USA, more than two million people are made ill every year with
antibiotic-resistant infections, with at least 23,000 dying as a result of
these infections (CDC, 2013). Food may act as a vector for the transfer
of antimicrobial resistant bacteria and antimicrobial resistance genes
to humans (Verraes et al., 2013). Multidrug-resistant (MDR) bacteria
can spread to humans either via the food supply (e.g., meat, fish, eggs
and dairy products), direct contact with animals or, more indirectly,
through environmental pathways (Angulo et al., 2004). The conse-
quences of antimicrobial resistance are particularly important when
pathogens are resistant to antimicrobials that are critically important
in the treatment of human disease. This concern includes infections ac-
quired in hospitals, community infections acquired in outpatient care
settings, and also, resistant foodborne disease associated with drug
use in food-producing animals (WHO, 2009).
The spread of MDR bacteria via meat and dairy products poses seri-
ous public health concerns. In the United States, the newly-released
10th National Antimicrobial Resistance Monitoring System (NARMS)
report describes alarming increases in antibiotic-resistant bacteria
found on retail meats. The report also confirmed that 80% of all antibi-
otics used in the United States are used not on humans but on food
animals, most of which are perfectly healthy (NARMS, 2011). The in-
creasing prevalence of multidrug resistance among Salmonella, not
only against the first-line antibiotics, ampicillin, chloramphenicol and
trimethoprim/sulfamethoxazole, but also, against clinically important
International Journal of Food Microbiology 189 (2014) 39–44
⁎ Corresponding author. Tel./fax: +81 82 424 7897.
E-mail address: tadashis@hiroshima-u.ac.jp (T. Shimamoto).
http://dx.doi.org/10.1016/j.ijfoodmicro.2014.07.031
0168-1605/© 2014 Elsevier B.V. All rights reserved.
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International Journal of Food Microbiology
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