MICROBIAL DRUG RESISTANCE

Volume 00, Number 00, 2018

ª Mary Ann Liebert, Inc.
DOI: 10.1089/mdr.2018.0121

Multiple Drug Resistance and Virulence Profiling

of Salmonella enterica Serovars Typhimurium
and Enteritidis from Poultry Farms of Faisalabad, Pakistan

Muhammad Wajid,1,2 Asad Bashir Awan,1,2 Muhammad Kashif Saleemi,3

Jörg Weinreich,4 Peter Schierack,4 Yasra Sarwar,1,2 and Aamir Ali1,2,4

The zoonotic serovars of Salmonella enterica particularly Typhimurium and Enteritidis pose a continuous
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global threat to poultry industry and public health. We report the prevalence of Salmonella Typhimurium and
Salmonella Enteritidis serovars in local poultry, phenotypic antimicrobial resistance profiling, and molecular
detection of antimicrobial resistance and virulence genes. A total of 340 clinical samples were collected and 239
carried Salmonella, which were identified by genus-specific PCR (invA gene) and by matrix-assisted laser
desorption/ionization time-of-flight. The 68 and 22 isolates were confirmed as Salmonella Typhimurium (stm
gene) and Salmonella Enteritidis (sdfI gene) respectively. Pulsed-field gel electrophoresis (PFGE) revealed 27
and 9 PFGE types of Salmonella Typhimurium and Salmonella Enteritidis respectively. Among 24 antimi-
crobials tested, highest resistance was observed against pefloxacin while highest susceptibility was found for
ertapenem in Salmonella Typhimurium and aztreonam in Salmonella Enteritidis. All isolates were found
multiple drug resistant, 98.8% as motile and 8.8% as extended spectrum beta lactamase producers. Most
prevalent resistance gene in Salmonella Typhimurium was parE (69.1%) while in Salmonella Enteritidis
blaTEM-1 (72.7%). High prevalence of SopE gene in Salmonella Typhimurium (91.1%) and Salmonella En-
teritidis (81.8%) indicated their zoonotic potential. The study is first of its kind from this region and highlights
the emerging trends of antimicrobial resistance of global concern.

Keywords: Salmonella, Typhimurium, Enteritidis, poultry, antimicrobial resistance, virulence profiling

Introduction prevalent in egg-laying poultry that led to illnesses related to

egg shells.6 Salmonellosis often occurs through contami-

T he genus Salmonella of the family Enterobacteri-

aceae has two species (Salmonella enterica and Sal-
monella bongori) with more than 2,600 serotypes.1
S. enterica can be broadly classified into typhoidal serotypes
including S. Typhi and S. Paratyphi A, B, and C, and non-
typhoidal salmonellae (NTS) including rest of the sero-
types.2 Among various poultry diseases, those caused by the
genus Salmonella are the most common and problematic in
terms of mortality, reduced growth, and loss of egg pro-
duction.3 The important zoonotic serovars infecting both
humans and animals include mainly S. enterica subsp. en-
terica serovar Typhimurium and S. enterica subsp. enterica
serovar Enteritidis.4 Different studies have reported Sal-
monella Typhimurium as the prevalent serotype isolated
from poultry meat5 while Salmonella Enteritidis found more
nated food, especially food products with an animal origin
and Salmonella have been reported more often from poultry
and poultry products than from any other food animals.7,8
The worldwide irrational use of antimicrobials in food-
animal production has led to the emergence of multiple
drug-resistant (MDR) Salmonella, which can be transmitted
to humans through food of animal origin.9 Among drug
resistance mechanisms, efflux pumps and extended spec-
trum beta lactamase (ESBL) production are gaining global
attention and an ever-growing burden in the community
across all ages.10,11
A little is known about the large-scale incidences of NTS
particularly in developing countries.12 In Pakistan, there is
no regulation or control for eradication of Salmonella from
poultry and the accurate diagnosis and targeted antibiotic

1
Health Biotechnology Division, National Institute for Biotechnology and Genetic Engineering, Faisalabad, Pakistan.
2
Pakistan Institute of Engineering and Applied Sciences, Islamabad, Pakistan.
3
Department of Pathology, Faculty of Veterinary Sciences, University of Agriculture, Faisalabad, Pakistan.
4
Institute for Biotechnology, Brandenburg University of Technology Cottbus-Senftenberg, Senftenberg, Germany.