Veterinary World, EISSN: 2231-0916
Available at www.veterinaryworld.org/Vol.11/October-2018/16.pdf
RESEARCH ARTICLE
Open Access
Antibiotic Susceptibility profile of Staphylococcus aureus isolated from
sausages in Meknes, Morocco
Abdelaziz Ed-Dra1, Fouzia Rhazi Filali1, Aziz Bouymajane1, Faouzia Benhallam1, Abdellah El Allaoui1, Abdellah Chaiba2 and
Filippo Giarratana3
1. Team of Microbiology and Health, Laboratory of Chemistry-Biology Applied to the Environment, Moulay Ismail
University Faculty of Science, BP. 11201 Zitoune Meknes, Morocco; 2. SADS–CRMEF Souss Massa Daraa Inezgane,
Agadir, Morocco; 3. Department of Veterinary Science, University of Messina, Polo Universitario della Annunziata,
98168 Messina, Italy.
Corresponding author: Abdelaziz Ed-Dra, e-mail: abdelaziz_iaa@yahoo.fr
Co-authors: FRF: fouzia.filali@yahoo.fr, AB: azizbouymajane.01@gmail.com, FB: f_benhallam@hotmail.com,
AEA: alaouixsaraa@hotmail.com, AC: abchaiba@yahoo.fr, FG: fgiarratana@unime.it
Received: 10-06-2018, Accepted: 16-08-2018, Published online: 19-10-2018
doi: 10.14202/vetworld.2018.1459-1465 How to cite this article: Ed-Dra A, Rhazi Filali F, Bouymajane A, Benhallam F,
El Allaoui A, Chaiba A, Giarratana F (2018) Antibiotic Susceptibility profile of Staphylococcus aureus isolated from sausages
in Meknes, Morocco, Veterinary World, 11(10): 1459-1465.
Abstract
Background and Aims: Staphylococcus aureus is one of the most common causes of foodborne disease worldwide, due to
the consumption of food contaminated by their toxins. This study aimed to determine the prevalence and the antimicrobial
resistance of S. aureus isolated from sausages in Meknes city of Morocco.
Materials and Methods: A total of 156 samples (Beef sausages, Turkey sausages, and Artisanal sausages “Merguez”) were
collected from different shopping sites (butchery, supermarket, street vendors, and weekly market “Souk”) and used for the
isolation of S. aureus. All the isolated strains were tested for their antimicrobials resistance to 16 antibiotics.
Results: Our results showed the presence of S. aureus in 63 samples (40.38%). Furthermore, the antimicrobial resistance
study showed that 84.13% of isolated S. aureus were resistant to streptomycin, 76.20% to tetracycline, 42.86% to ampicillin,
41.27% to doxycycline, 38.1% to penicillin G, and 19.05% to chloramphenicol with the presence of 25 different phenotypic
profiles. However, all isolated strains were sensitive to oxacillin, cefoxitin, gentamicin, and vancomycin.
Conclusion: The findings of this study revealed consumption of sausages as a potential risk of foodborne poisonings
because of its contamination with the multi-resistant strains of S. aureus. Moreover, this contamination is related to the
season, sampling sites and the origin of the raw material.
Keywords: antimicrobial resistance, foodborne disease, infection, sausages, Staphylococcus aureus.
Introduction
Foodborne diseases are a major public health
concern worldwide and are defined as a disease of
infectious or toxic nature caused by, or thought to be
caused by, the consumption of contaminated food or
water [1]. Staphylococcal foodborne disease is one
of the most frequent universal foodborne diseases,
and it is caused by the ingestion of food contaminated with enterotoxins produced by some strains of
Staphylococcus [2,3]. Its symptoms have a rapid onset
(2-6 h) and may include vomiting, stomach pain, and
diarrhea [4].
The genus Staphylococcus is placed in the
family Micrococcaceae. This genus is divided into
coagulase-positive staphylococci and coagulase-negative staphylococci based on their ability to coagulate plasma [5]. Staphylococcus aureus is the most
Copyright: Ed-Dra, et al. Open Access. This article is distributed
under the terms of the Creative Commons Attribution 4.0
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License
(http://creativecommons.org/licenses/
by/4.0/), which permits unrestricted use, distribution, and
reproduction in any medium, provided you give appropriate credit
to the original author(s) and the source, provide a link to the
Creative Commons license, and indicate if changes were made.
The Creative Commons Public Domain Dedication waiver (http://
creativecommons.org/publicdomain/zero/1.0/) applies to the data
made available in this article, unless otherwise stated.
Veterinary World, EISSN: 2231-0916
significant human pathogen among the staphylococci. It is a ubiquitous spherical bacterium, Grampositive and facultative anaerobic. He can grow in a
wide range of pH (between 4.2 and 9.3), temperatures
(between 7°C and 48.5°C), and in a high concentration
of sodium chloride (15%) [1]. These characteristics
favor the growth of this bacterium in many food products. Indeed, previous studies have isolated S. aureus
from various food of animal origin [6-12].
Worldwide, S. aureus is considered the third
common pathogen that causes food poisoning [13].
In the United States, S. aureus is considered one of
the top five pathogens causing domestically acquired
foodborne diseases and is responsible for an estimate of 241,000 illnesses per year [10,14]. In 2009,
23 cases of food poisoning were reported in France
due to the consumption of raw milk and cheese contaminated with S. aureus [15]. A study in Morocco
showed that S. aureus was responsible for 72% of
foodborne outbreaks [16]. Moreover, the delegation
of epidemiology and disease control reported 13,339
cases of foodborne diseases between 2001 and 2010
of which 31% were caused by S. aureus [17].
The extended use and misuse of antibiotics in
agriculture, stock farming, veterinary medicine, and
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treatment of human diseases increase the resistance of
bacteria to antimicrobial agents. In livestock farms,
different antimicrobial agents are used extensively
in sub-therapeutic/therapeutic doses for growth promotion, routine disease prevention, and treatment of
bacterial diseases [18,19]. This indiscriminate practice is usually worse in developing countries including Morocco, where there are no strict controls on the
use of antimicrobials in food-producing animals [20].
This has led to increased resistance to different antimicrobials used in these fields [11,21-23]. In the last
years, S. aureus resistant to methicillin (MRSA) and
vancomycin (VRSA) was isolated from different samples [1,7,8,10,21,23-26], these antibiotics are a choice
drug for the treatment of cases infected by this bacterium; hence, the World Health Organization has
triggered the alarm signal about these resistances and
ranked the MRSA and VRSA among the high priority
for searching the new and effective antibiotic treatments [27].
In this context, this study aimed to evaluate the
prevalence of S. aureus in sausages sold in Meknes
city (Morocco) and to determine the antimicrobial
susceptibility of isolated strains.
Materials and Methods
Ethical approval
Ethical approval was not required in this study
since no live animals were used in the experiments.
Samples collection and microbiological analysis
A total of 156 samples of sausages distributed
as follow: 60 of turkey sausages, 60 of beef sausages,
and 36 of “Merguez” sausages were randomly collected from various local supermarkets, weekly market, butcheries, and street vendors. The collection was
carried out during 1 year from March 2014 to February
2015. The samples were aseptically collected, and
each sample was placed in a separate, sterile plastic
bag. The samples were brought under refrigeration to
the laboratory and analyzed within the following 2 h.
The samples (25 g) were weighed into sterile stomacher bags diluted with 225 mL sterile buffered peptone water (Biokar) and homogenized in a stomacher
for about 1 min; 0.1 mL was streaked on Baird-Parker
(BP) agar (Biokar) supplemented with egg yolk tellurite emulsion and incubated at 37°C for 24-48 h.
Strains cultured on BP agar medium were identified
as S. aureus if growth was observed and the colonies
showed the typical morphologic characteristics (black
colonies with an opaque precipitation halo). The tube
coagulate test was determined and evaluated for coagulation after 3 and 24 h of incubation.
Antibiotic susceptibility
The resistance pattern of S. aureus was determined using the disk-diffusion test [28]. 16 antibiotics
(Oxoid) were chosen for the study based on the most
used active principles in human medicine, national
veterinary therapy, and according to their common use
Veterinary World, EISSN: 2231-0916
in research. The use of oxacillin/methicillin is not usually used in veterinary practice, and it was included
in this study only for epidemiological purposes; the
drugs tested are indicated in Table-1. Multiple antibiotic resistance (MAR) index is calculated as the ratio
of some resistance antibiotics to the total number of
antibiotics to which the isolates are exposed. S. aureus
ATCC 29213 was used as a control strain.
Statistical analysis
The data were presented as means±standard
error, and the statistical analyses were performed
using Microsoft Office Excel (2010). The comparison
of contamination averages was performed using the
student test with p<0.05 .
Results
Contamination rate of sausages by staphylococci
This study was carried out during 1 year to evaluate the contamination level of sausages by staphylococci, and to study the effect of the different factors
influencing this contamination. The results of this
study show that the average rate of contamination with
staphylococci was 3.42±0.88 log cfu/g with a minimum value of 1.47 log cfu/g and a maximum value
of 5.6 log cfu/g. The study of seasonal effect shows
that staphylococci take a maximum value during
autumn (4.15±0.86 log cfu/g), followed by summer
(3.68±0.78 log cfu/g), winter (3.00±0.46 log cfu/g),
and spring (2.90±0.71 log cfu/g) (Figure-1), with
a significant difference between the cold seasons
(winter and spring) and the hot seasons (autumn
and summer) (p<0.05). Furthermore, the study of
the sampling sites effect shows that sausages sold at
street vendors are the most contaminated with staphylococci (3.82±0.84 log cfu/g), followed by souk
(3.6±0.61 log cfu/g), butchery (3.5±0.88 log cfu/g),
and the supermarket (2.51±0.46 log cfu/g) (Figure-2),
while the sausages sold in supermarket differ significantly from those sold in the others sites (p<0.05). In
the other hand, the result of this study showed that
Table-1: Antimicrobial agents and the range of
concentrations tested.
Antimicrobial agents
Code
Penicillin G
Ampicillin
Oxacillin
Cefoxitin
Gentamicin
Kanamycin
Fusidic acid
Ofloxacin
Enrofloxacin
Erythromycin
Tetracycline
Doxycycline
Vancomycin
Chloramphenicol
Streptomycin
Trimethoprim-sulfamethoxazole
P
AMP
OX
FOX
GN
K
FD
OFX
ENR
E
TE
DXT
VA
C
S
SXT
Concentration
disc (µg)
6
10
5
30
30
30
10
5
5
15
30
30
30
30
10
1.25/23.75
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the raw material origin has a significant effect on
the contamination rate of sausages by staphylococci
(p<0.05); the artisanal sausages “Merguez” is the
most contaminated (3.82±0.84 log cfu/g), followed
by beef sausages (3.5±0.93 log cfu/g) and turkey sausages (3.15±0.75 log cfu/g) (Figure-3).
furthermore, the study of sampling sites effect showed
that the sausages sold in street vendors were the most
contaminated with 50% (Table-3). On the other hand,
the artisanal sausages “Merguez” was the most contaminated with S. aureus according to the raw material
origin (Table-4).
Prevalence of S. aureus in sausage samples
Antibiotic susceptibility test
The isolation and identification of S. aureus
were performed according to the method described
previously. From 156 analyzed samples, 63 were
positive for S. aureus (40.38%). These results showed
that S. aureus governs the summer season (Table-2);
Figure-1: The average values of staphylococci counted in
sausages according to seasons sampling.
The antibiotic susceptibly was carried out
according to the method described by the Clinical
Laboratory Standard Institute. The isolated S. aureus
(63) was tested for 16 antibiotics belonging to different groups, and the results are presented in Table-5.
This results showed that 61 isolates (96.82%) were
resistant to at least one antibiotic, 56 (88.88%) were
resistant to two or more antibiotics, and 44 (69.84%)
were resistant to three or more antibiotics (considered as Multi-resistant). Moreover, the analysis of our
results showed that the MAR index varies between 0
and 0.56 with the presence of 25 different phenotypic
profiles (Table-6).
Among the tested antibiotics, the isolated strains
were resistant to streptomycin (84.13%), followed by
tetracycline (76.20%), ampicillin (42.86%), doxycycline (41.27%), and penicillin G (38.1%). On the other
hand, they were sensitive to oxacillin, cefoxitin, gentamicin, and vancomycin (Table-5).
Table-2: Effect of sampling seasons on sausages
contamination with S. aureus.
Sampling
seasons
Spring
Summer
Autumn
Winter
Number of samples
Analyzes
Positives
Percentage
39
39
39
39
16
29
14
4
41.02
74.36
35.89
10.25
S. aureus=Staphylococcus aureus
Figure-2: The average values of staphylococci counted in
sausages according to sampling sites.
Table-3: Effect of sampling sites on sausages
contamination with S. aureus.
Sampling sites
Butchery
Supermarket
Street vendors
Weekly market
Number of samples
Analyzes
Positives
Percentage
72
24
36
24
28
3
18
14
38.88
12.5
50
58.33
S. aureus=Staphylococcus aureus
Table-4: Effect of raw material origin on sausages
contamination with S. aureus.
Origin
Figure-3: The average values of staphylococci counted in
sausages according to sausages types.
Veterinary World, EISSN: 2231-0916
Turkey sausage
Beef sausage
Artisanal sausages
“Merguez”
Number of samples
Analyzes
Positives
Percentage
60
60
36
22
23
18
36.66
38.33
50
S. aureus=Staphylococcus aureus
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Table-5: Antimicrobial resistance percentages of isolated S. aureus.
Antibiotics
Number of S. aureus isolates (n=63)
Penicillin G (6 µg)
Ampicillin (10 µg)
Oxacillin (5 µg)
Cefoxitin (30 µg)
Gentamicin (30 µg)
Kanamycin (30 µg)
Fusidic acid (10 µg)
Ofloxacin (5 µg)
Enrofloxacin (5 µg)
Erythromycin (15 µg)
Tetracycline (30 µg)
Doxycycline (30 µg)
Vancomycin (30 µg)
Chloramphenicol (30 µg)
Streptomycin (10 µg)
Trimethoprim-sulfamethoxazole (1.25 µg/23.75 µg)
P
AMP
OX
FOX
CN
K
FD
OFX
ENR
E
TE
DXT
VA
C
S
SXT
S (%)
R (%)
39 (61.9)
36 (57.14)
63 (100)
63 (100)
63 (100)
59 (93.65)
62 (98.41)
54 (85.71)
54 (85.71)
60 (95.24)
15 (23.80)
37 (58.73)
63 (100)
51 (80.95)
10 (15.87)
61 (96.82)
24 (38.1)
27 (42.86)
0 (0)
0 (0)
0 (0)
4 (6.35)
1 (1.59)
9 (14.29)
9 (14.29)
3 (4.76)
48 (76.20)
26 (41.27)
0 (0)
12 (19.05)
53 (84.13)
2 (3.18)
S. aureus=Staphylococcus aureus
Table-6: Resistance profile of isolated S. aureus.
Number of antibiotics
0
1
2
3
4
5
6
7
9
Resistance profile
TE
S
S, TE
TE, C
OFX, ENR
S, AMP
S, AMP, P
S, TE, DXT
S, TE, C
S, TE, SXT
S, TE, DXT, C
S, TE, DXT, SXT
S, TE, OFX, ENR
S, TE, DXT, AMP, P
S, TE, DXT, C, P
S, AMP, OFX, ENR, K
TE, DXT, AMP, P, E
TE, DXT, OFX, ENR, E
S, TE, DXT, C, FD
S, TE, DXT, AMP, C
S, TE, AMP, P, ENR, OFX
S, TE, DXT, AMP, P, K
S, TE, AMP, P, OFX, ENR, K
S, TE, DXT, AMP, P, C, OFX, ENR, E
Number of Isolates
MAR
2
4
1
9
1
1
1
9
6
2
1
4
1
1
7
2
1
1
1
1
1
2
1
2
1
0
0.06
0.06
0.125
0.125
0.125
0.125
0.19
0.19
0.19
0.19
0.25
0.25
0.25
0.31
0.31
0.31
0.31
0.31
0.31
0.31
0.37
0.37
0.43
0.56
MAR=Multiple antibiotic resistance index, S=Streptomycin, TE=Tetracycline, AMP=Ampicillin, P=Penicillin G,
C=Chloramphenicol, OFX=Ofloxacin, ENR=Enrofloxacin, K=Kanamycin, E=Erythromycin, DXT=Doxycycline,
FD=Fusidic acid, SXT=Trimethoprim-Sulfamethoxazole. S. aureus=Staphylococcus aureus
Discussion
The genus Staphylococcus includes at least 40
species which are pathogenic bacteria causing a broad
spectrum of diseases with varying degrees of severity;
their natural habitat includes humans, animals, and
environment. The presence of staphylococci in food
is considered a major risk to the public health, for this
reason, its limit of acceptability in sausages was fixed
at 5.103 cfu/g in Morocco.
The results of our study showed that the contamination rate of sausages with staphylococci has an
Veterinary World, EISSN: 2231-0916
average rate of 3.42±0.88 log cfu/g with a minimum
of 1.47 log cfu/g and a maximum of 5.6 log cfu/g,
of which 31.41% exceeds the limit and are unfit for
consumption. These results are similar to those found
in Turkey [29], lower than those reported in Nigeria
[30], and higher than the results carried out in Jordan
[31]. However, a study carried out previously in Rabat
city (Morocco) showed that the contamination of
poultry meat with staphylococci has an average rate
of 2.67 log cfu/g [32].
Our finding showed the presence of S. aureus
in 63 samples (40.38%). These results are similar
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to that found in the imported meats in South Korea
(40.94%) [15] and fresh sausages samples in Egypt
(45%) [33]. They are higher than that reported in
poultry meat in Rabat city of Morocco (16.66%) [32],
chicken samples in China (24.2%) [23], analyzed
meat samples in Italy (10%) [34], and fresh meat
samples in Shanghai (28.1%) [35]. However, they
are lower than that reported in turkey samples in the
USA (64.2%) [10]. In Italy, the results published by
Pesavento et al. [6] showed the presence of S. aureus in
23.86% of analyzed samples, with 28.57% in poultry
meat, 29.41% in beef meat, and 15.15% in pork meat.
The high contamination of sausages with S. aureus
may occur directly from contaminated raw material
or may results from poor hygiene during production
processes or at the retail and storage stage [36].
The massive use of antibiotics in feed to promote
growth and the inappropriate use of antimicrobials
agents in veterinary and human medicine are considered to be major contributors to the emergences of
resistance [20,37]. Moreover, S. aureus is notorious for
its ability to become resistant to antimicrobials due to
their capacity to produce an exopolysaccharide barrier
and because of their location within microabscesses,
which limit the action of drugs [38]. In the other hand,
the acquisition of resistance genes by horizontal transfer has high importance; some studies prove the presence of different genes such as tetM, mecA, and blaZ
that are responsible for the resistance to tetracycline,
oxacillin, and penicillin, respectively [39].
The results of our study showed that 96.82% of
isolated S. aureus were resistant to at least one antibiotic, 88.88% were resistant to two or more antibiotics,
and 69.84% were resistant to three or more antibiotics.
A study in Italy showed that 68.8% of analyzed S. aureus
were resistant to at least one antibiotic [34]. In Jordan,
about 88.5% of the S. aureus exhibited resistance to at
least one antibiotic in imported fresh fish samples [40].
In the United States, 52% of the S. aureus isolated from
meat and poultry samples were multi-resistant [19].
The antimicrobial analysis showed that 84.13%
of isolated S. aureus are resistant to streptomycin,
this result is higher than that found in retail chicken
in Egypt (52.1%) [41], and in food samples in Iran
(5.8%) [39]. Furthermore, 76.20% of isolated strains
were resistant to tetracycline; this result is similar to
that found in retail chicken in Egypt taking in consideration the intermediate and resistance profiles [41],
but higher than that found in Italy (19.04%) [6],
Jordan (36.5%) [39], and Iran (29.6%) [42].
The rate of resistance to ampicillin and penicillin
G was 42.86% and 38.1%, respectively. The resistance
to these antibiotics is common in S. aureus and has
been observed previously in Malaysia (72.30% ampicillin and 53.38% penicillin) [43], Iran (77.3% ampicillin and 76% penicillin G) [44], and Italy (42.86%
ampicillin and 16.66% penicillin G) [6]. On the other
hand, the isolated strains of S. aureus were sensitive
to gentamicin, oxacillin, cefoxitin, and vancomycin.
Veterinary World, EISSN: 2231-0916
The high percentage of resistant S. aureus isolates to these antibiotics could be due to the widespread
administration of these antimicrobials to control and
treat infections on dairy farms [39]. Furthermore,
MAR index analysis showed the presence of 25 different phenotypic profiles among the 63 strains. This
diversity can be explained by the different sources
of contamination of sausages since the preparation
of the raw material (slaughter, evisceration, cutting)
until the manufacturing, storage, and sales in different
sites [36,45].
Conclusion
The high level of contamination of sausages
with S. aureus highlights the poor hygiene all along
the chain of manufacture and sale of this product.
Furthermore, our study showed that the consumption
of this product might be a potential risk of foodborne
infection. Fortunately, we have not found strains resistant to methicillin and vancomycin, but this resistance
can be acquired from the medical or veterinary fields
to the food chain product. Hence, it is interesting to
survey the resistance profile of this bacterium in all
the stage manufacturing process and applied the good
practices of hygiene and Hazard Analysis Critical
Control Point especially in informal sales sites.
Authors’ Contributions
This work was carried out in collaboration
between all authors. AE, FRF, and FB designed the
experimental procedures. AE, AB, AEA, and AC
conducted the experimental analysis. AE, FRF, and
FG analyzed the data and wrote the manuscript. All
authors read and approved the final manuscript.
Acknowledgments
The authors thank the members of the regional
laboratory of epidemiological diagnosis and environmental hygiene of Meknes-Tafilalet Region for the
help in sampling and microbiological analysis. The
authors declare that they did not receive any funding
source to support this study.
Competing Interests
The authors declare that they have no competing
interests.
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