Antibiotic resistance determinants and genetic analysis of Salmonella
enterica isolated from food in Morocco
Manuela Murgia
a,
⁎, Brahim Bouchrif
b
, Mohammed Timinouni
c
, Ahmed Al-Qahtani
d
,
Mohammed N. Al-Ahdal
d
, Pietro Cappuccinelli
a
, Salvatore Rubino
a,d
, Bianca Paglietti
a
a
Department of Biomedical Sciences, University of Sassari, V. le San Pietro 43/B, 07100 Sassari, Italy
b
Laboratoire de microbiologie et d'hygiène des aliments et des eaux, Institut Pasteur in Morocco, 1 place Louis Pasteur, Casablanca 20100, Morocco
c
Laboratoire de microbiologie et biologie moléculaire, Institut Pasteur in Morocco, 1 place Louis Pasteur, Casablanca 20100, Morocco
d
Department of Infection and Immunity, King Faisal Specialist Hospital and Research Centre, P.O. Box 3354 (MBC-03), Riyadh 11211, Saudi Arabia
abstract article info
Article history:
Received 12 March 2015
Received in revised form 21 July 2015
Accepted 7 August 2015
Available online 9 August 2015
Keywords:
Salmonella
PFGE
MLST
Antibiotic-resistance determinants
Antimicrobial-resistant non-typhoidal Salmonella (NTS) are an important cause of infection in Africa, but there is
a lack of information on their molecular mechanisms of resistance and epidemiology. This study contributes to fill
this gap through the characterization by pulsed-field gel electrophoresis (PFGE), multilocus sequence typing
(MLST), plasmid profiling and analysis of antibiotic-resistance determinants of 94 Salmonella enterica strains
isolated from food in Morocco. PFGE revealed considerable heterogeneity among the strains, showing 32
pulsotypes. MLST of strains representative of the different serovars evidenced 13 sequence types (STs), three
of which were newly identified (ST1694, ST1768 and ST1818) and nine not previously reported in Morocco.
Thirty-four strains harbored from one to four plasmids, of IncI1 group in S. Mbandaka, IncFIIA in S. Typhimurium,
IncL/M in S. Hadar and S. Blockley. For the first time in Morocco an intact Salmonella Genomic Island 1 (SGI1)
carrying the resistance genes aadA2, floR, tetG, bla
PSE-1
and sul1 was detected in S. Typhimurium DT104. In serovar
Hadar resistance to ampicillin, tetracycline and streptomycin was associated to bla
TEM-1
, tetA and strA
genes respectively, whereas one mutation in gyrA (Asp87Asn) and one in parC (Thr54Ser) genes conferred resis-
tance to nalidixic acid. These findings improve the information on foodborne Salmonella in Morocco, evidencing
the presence of MDR strains potentially dangerous to humans, and provide useful data for future studies.
© 2015 Elsevier B.V. All rights reserved.
1. Introduction
Non-typhoidal Salmonella (NTS) are one of the most frequent causes
of foodborne diseases worldwide, with severe public health consequences
(Rabsch et al., 2001). It is estimated that every year 94 million persons
contract NTS infections, with about 155,000 deaths (http://www.who.
int/drugresistance/documents/surveillancereport/en/).
Although uncomplicated NTS gastrointestinal infections do not
require antimicrobial treatment, in most severe cases (e.g., acute diarrhea,
high fever and systemic infection) an appropriate antimicrobial therapy is
needed (Gordon, 2008; Morpeth et al., 2009; Reddy et al., 2010), and the
drugs of choice are fluoroquinolones for adults and third-generation
cephalosporins for children (White et al., 2001). The selective pressure
due to the misuse of antibiotics in humans and domestic livestock has
led to the emergence of antibiotic resistance in zoonotic bacteria, and
multidrug-resistant (MDR) Salmonella are increasingly isolated from
different food products worldwide (Ben Aissa and Al-Gallas, 2008;
Bouchrif et al., 2009b; Threlfall et al., 2000). Multiple resistance genes,
incorporated into integrons or transposons, can be easily exchanged
among Salmonella and other bacteria through genetic mobile elements,
causing the rapid dissemination of MDR strains (Guerra et al., 2000;
Michael et al., 2006). A well-known example is the Salmonella Genomic
Island 1 (SGI1), related to the wide spread of MDR S. Typhimurium
DT104 epidemic strains and described in different Salmonella serovars
(Boyd et al., 2001; Levings and Lightfoot, 2005). Conjugative plasmids
are also actively involved in the transmission of resistance genes,
as reported for the IncI1 plasmids associated to the dissemination
of β-lactamase genes among Salmonella from food of animal origin
(Cloeckaert et al., 2007; García-Fernández et al., 2008). Infections
caused by multidrug-resistant NTS are more acute and invasive,
and therapeutic failures due to antimicrobial resistance increase the risk
of death, especially in developing countries where alternative treatments
are often unavailable (http://www.who.int/drugresistance/documents/
surveillancereport/en/).
International Journal of Food Microbiology 215 (2015) 31–39
⁎ Corresponding author.
E-mail addresses: murgiam@uniss.it (M. Murgia), brahim.bouchrif@pasteur.ma
(B. Bouchrif), mohammed.timinouni@pasteur.ma (M. Timinouni), aqahtani@kfshrc.edu.sa
(A. Al-Qahtani), drahdal@gmail.com (M.N. Al-Ahdal), pcappuc@uniss.it (P. Cappuccinelli),
rubino@uniss.it (S. Rubino), biancap@uniss.it (B. Paglietti).
http://dx.doi.org/10.1016/j.ijfoodmicro.2015.08.003
0168-1605/© 2015 Elsevier B.V. All rights reserved.
Contents lists available at ScienceDirect
International Journal of Food Microbiology
journal homepage: www.elsevier.com/locate/ijfoodmicro