Acta Tropica 111 (2009) 144–149
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Acta Tropica
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Genetic basis of multidrug resistance in Salmonella enterica serovars Enteritidis
and Typhimurium isolated from diarrheic calves in Egypt
Ashraf M. Ahmed
a
, Emad E.A. Younis
b
, Yojiro Ishida
c
, Tadashi Shimamoto
c,∗
a
Department of Bacteriology, Mycology and Immunology, Faculty of Veterinary Medicine, Kafr El-Sheikh University, Kafr El-Sheikh 33516, Egypt
b
Department of Internal Medicine, Infectious and Fish Diseases, Faculty of Veterinary Medicine, Mansoura University, Mansoura 35516, Egypt
c
Laboratory of Food Microbiology and Hygiene, Graduate School of Biosphere Science, Hiroshima University, Higashi-Hiroshima 739-8528, Japan
article info
Article history:
Received 25 September 2008
Received in revised form 6 April 2009
Accepted 8 April 2009
Available online 16 April 2009
Keywords:
Integron
-Lactamase
Multidrug resistance
qnr
Salmonella
abstract
Up to this date, nothing is known about the molecular basis of antimicrobial resistance in Salmonella
isolated from animals in Africa. Therefore, this study was carried out to screen the incidence of multidrug-
resistant (MDR) strains of Salmonella from neonatal calf diarrhea in Egypt and also to characterize the
molecular basis of this resistance. Nine unique Salmonella isolates were obtained from 220 fecal sam-
ples, and six of these showed multidrug resistance phenotypes and harbored at least two antimicrobial
resistance genes. Four were Salmonella enterica serovar Typhimurium and two were S. enterica serovar
Enteritidis. Class 1 integrons were identified in all MDR Salmonella isolates. The identified gene cassettes
within class 1 integrons were as follows; aminoglycoside adenyltransferase type A (aadA1, aadA2 and
aadA5), which confer resistance to streptomycin and spectinomycin, and dihydrofolate reductase gene
cassettes (dfrA1, dfrA15 and dfrA15), which confer resistance to trimethoprim. A class 2 integron contain-
ing dfrA1-sat2-aadA1 gene cassettes was identified in only one isolate of S. enterica serovar Enteritidis.
The -lactamase-encoding gene, bla
TEM-1
, was identified in five isolates and the extended-spectrum -
lactamase-encoding genes, bla
CMY-2
and bla
SHV-12
, were identified in S. enterica serovar Typhimurium.
Furthermore, the plasmid-mediated quinolone resistance genes, qnrB, qnrS and aac(6
′
)-Ib-cr, were also
identified. To the best of our knowledge, this is the first report of qnrS in S. enterica serovar Enteritidis, qnrB
in S. enterica serovar Typhimurium, and aac(6
′
)-Ib-cr in Salmonella of animal origin. Also, this is the first
report of the molecular characterization of antimicrobial resistance in Salmonella isolated from animals
in Africa.
© 2009 Elsevier B.V. All rights reserved.
1. Introduction
Salmonella is one of the most important pathogens responsible
for gastrointestinal infections in animals and humans. The genus
Salmonella belongs to the family Enterobacteriaceae and consists of
six subgroups. Currently, over 2,500 serovars have been identified
in this genus and 99% of the serovars responsible for diseases in
warm-blooded animals are members of group I (Salmonella enterica
subsp. enterica)(Bopp et al., 2003). S. enterica is a zoonotic bacteria
transmitted through the food chain, and is an important cause of
disease in humans, with 95% of cases estimated to be of food-borne
origin (Mead et al., 1999). In cattle, Salmonella affects both adults
and calves but the greatest mortality occurs in the young, with most
calves affected between 10 days and 3 months of age (Rings, 1985).
Antimicrobials are used in food animals to treat or prevent
disease and also to promote growth. Antimicrobial resistance is
∗
Corresponding author. Tel.: +81 82 424 7897; fax: +81 82 424 7897.
E-mail address: tadashis@hiroshima-u.ac.jp (T. Shimamoto).
emerging as a serious public health concern (Martinez and Baquero,
2002). In addition to the human health concerns, antimicrobial-
resistant pathogens also pose a severe and costly animal health
problem, by prolonging illness and decreasing productivity through
higher morbidity and mortality rates. Food animals and foods of
animal origin are traded worldwide. Thus, the occurrence of antimi-
crobial resistance in one country is a problem for all countries.
Strains of Salmonella that are resistant to antimicrobial agents have
been reported worldwide (Angulo and Griffin, 2000; Breuil et al.,
2000; van Duijkeren et al., 2003).
Several studies have reported on the molecular basis of resis-
tance in Salmonella isolated from animals worldwide (Winokur et
al., 2000; Yang et al., 2002; Ria ˜ no et al., 2006; van Essen-Zandbergen
et al., 2007; Ahmed et al., 2009). However, little is known about
the molecular basis of this resistance from cases of calf diarrhea.
Furthermore, till date, nothing is known about the molecular basis
of antimicrobial resistance in Salmonella isolated from animals in
Africa. Here, we investigated the presence of multidrug-resistant
(MDR) strains of Salmonella isolated from diarrheic calves in Egypt
and performed genetic analysis on this resistance.
0001-706X/$ – see front matter © 2009 Elsevier B.V. All rights reserved.
doi:10.1016/j.actatropica.2009.04.004