Next Article in Journal
Immunosuppression in Malaria: Do Plasmodium falciparum Parasites Hijack the Host?
Next Article in Special Issue
Identification of cbiO Gene Critical for Biofilm Formation by MRSA CFSa36 Strain Isolated from Pediatric Patient with Cystic Fibrosis
Previous Article in Journal
Epstein-Barr Virus Promotes Tumor Angiogenesis by Activating STIM1-Dependent Ca2+ Signaling in Nasopharyngeal Carcinoma
Previous Article in Special Issue
Ecology and Genetic Lineages of Nasal Staphylococcus aureus and MRSA Carriage in Healthy Persons with or without Animal-Related Occupational Risks of Colonization: A Review of Global Reports
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Pathogens
Volume 10
Issue 10
10.3390/pathogens10101276
pathogens-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Molecular Characterization of Staphylococcus aureus Isolated from Human and Food Samples in Northern Algeria

by
Rachid Achek
1,2,
Hosny El-Adawy
3,4,*,
Helmut Hotzel
3,
Ashraf Hendam
5,
Herbert Tomaso
3,
Ralf Ehricht
6,7,8,
Heinrich Neubauer
3,
Ibrahim Nabi
9,
Taha Mossadak Hamdi
2 and
Stefan Monecke
6,7,10
1
Faculty of Nature and Life and Earth Sciences, Djilali-Bounaama University, Soufay, Khemis-Miliana 44225, Algeria
2
Laboratory of Food Hygiene and Quality Assurance System, High National Veterinary School, Oued Smar, Algiers 16059, Algeria
3
Institute of Bacterial Infections and Zoonoses, Friedrich-Loeffler-Institut, 07743 Jena, Germany
4
Faculty of Veterinary Medicine, Kafrelsheikh University, Kafr El-Sheikh 35516, Egypt
5
Climate Change Information Center, Renewable Energy and Expert Systems (CCICREES), Agricultural Research Center, 9 Algamaa Street, Giza 12619, Egypt
6
Leibniz Institute of Photonic Technology (IPHT), 07745 Jena, Germany
7
InfectoGnostics Research Campus Jena e. V., 07743 Jena, Germany
8
Institute of Physical Chemistry, Friedrich Schiller University Jena, 07743 Jena, Germany
9
Faculty of Sciences, Yahia Farès University, Urban Pole, Médéa 26000, Algeria
10
Institute for Medical Microbiology and Virology, Dresden University Hospital, 01307 Dresden, Germany
*
Author to whom correspondence should be addressed.
Pathogens 2021, 10(10), 1276; https://doi.org/10.3390/pathogens10101276
Submission received: 1 September 2021 / Revised: 23 September 2021 / Accepted: 28 September 2021 / Published: 3 October 2021
(This article belongs to the Special Issue Staphylococcus Infections in Humans and Animals)
Browse Figure
Versions Notes

Abstract

:
Staphylococcus aureus is a commensal resident of the skin and nasal cavities of humans and can cause various infections. Some toxigenic strains can contaminate food matrices and cause foodborne intoxications. The present study aimed to provide relevant information (clonal complex lineages, agr types, virulence and antimicrobial resistance-associated genes) based on DNA microarray analyses as well as the origins and dissemination of several circulating clones of 60 Staphylococcus aureus isolated from food matrices (n = 24), clinical samples (n = 20), and nasal carriers (n = 16) in northern Algeria. Staphylococcus aureus were genotyped into 14 different clonal complexes. Out of 60 S. aureus, 13 and 10 isolates belonged to CC1-MSSA and CC97-MSSA, respectively. The CC 80-MRSA-IV was the predominant S. aureus strain in clinical isolates. The accessory gene regulator allele agr group III was mainly found among clinical isolates (70.4%). Panton–Valentine leukocidin genes lukF/lukS-PV were detected in 13.3% of isolates that all belonged to CC80-MRSA. The lukF/S-hlg, hlgA, and hla genes encoding for hemolysins and leucocidin components were detected in all Staphylococcus aureus isolates. Clinical and food isolates harbored more often the antibiotic resistance genes markers. Seventeen (28.3%) methicillin-resistant Staphylococcus aureus carrying the mecA gene localized on a SCCmec type IV element were identified. The penicillinase operon (blaZ/I/R) was found in 71.7% (43/60) of isolates. Food isolates belonging to CC97-MSSA carried several antibiotic resistance genes (blaZ, ermB, aphA3, sat, tetM, and tetK). The results of this study showed that all clones were found in their typical host, but interestingly, some nasal carriers had isolates assigned to CC705 thought to be absent in humans. The detection of MRSA strains among food isolates should be considered as a potential public health risk. Therefore, controlling the antibiotics prescription for a rational use in human and animal infections is mandatory.

1. Introduction

Staphylococcus aureus is a Gram-positive bacterium, considered as a commensal resident of the skin and nasal cavities of humans and animals. This bacterium can spread from its habitual niches to other parts of the body and cause various clinical infections [1,2] and foodborne intoxications [3].
The pathogenic potential of S. aureus is essentially related to an arsenal of virulence factors and the capacity of acquiring resistance to different antibiotics [4,5]. The emergence of resistance to methicillin, and beta-lactams in general, has made methicillin-resistant S. aureus (MRSA) a serious public health problem [6].
The genetic background of S. aureus was intensively investigated using different typing tools such as pulsed-field gel electrophoresis (PFGE), spa-typing, multilocus sequence typing (MLST), whole genome sequencing, and DNA microarray-based analysis [7,8,9]. The study of the clonal diversity among S. aureus using molecular techniques contributed to our understanding of the genetic diversity of S. aureus and provided insights into the origin and spread of MRSA into humans and animals [10,11].
The clonal complexes (CC) CC5, CC8, CC22, CC30, and CC45, are typically hospital-associated MRSA (HA-MRSA) infections [11], while the lineages CC1, CC8, CC30 and CC80 have found to be mainly community-acquired MRSA (CA-MRSA) infections [12]. CC398 and CC9 have emerged as livestock-associated MRSA (LA-MRSA) [13,14].
The spread of specific clones differed depending on geographical regions. The sequence type (ST) ST80 was predominant in North African countries [15,16,17]. ST 8 (USA300) and ST1 (USA400) are prevalent in North America [18] and the Panton–Valentine leukocidin (PVL) positive ST93, known as “Queensland CA-MRSA”, in Australia [19]. However, some clones or lineages of S. aureus are not restricted to a specific host and can be found to colonize or cause infections in a broad variety of animal species, including humans [20,21]. The CC398 is associated with livestock, but is also able to colonize humans [22].
Panton–Valentine leukocidin (PVL) is a phage-borne toxin killing immune cells and causing tissue necrosis. PVL is a bi-component toxin forming polymeric pores in the membranes of target cells. It is structurally related to lukM/lukF-P83 from ruminant strains of S. aureus, which is also phage-borne. Other, similar bicomponent leukocidins in S. aureus are lukF/S-hlg (on the gamma hemolysin locus), lukD/E (on a genomic island), and lukA/B (synonyms: lukX/Y, lukG/H), which belong to the core genomic and can be considered as a species-specific marker of S. aureus. PVL genes are frequently found among community-acquired MRSA strains [23]. These strains are typically associated with severe skin and soft tissue infections [24].
The emergence of PVL-positive MRSA was previously detected in hospitals and communities in northern Africa in Algeria, Tunisia, and Egypt [16,17,25], in central Africa in São Tome and Príncipe, Nigeria, Ghana, and Kenya [26,27,28,29]) and in southern African countries such as South Africa [30]. CC80 was predominant in North African countries and CC88 was predominant in Sub-Saharan countries. CC5 was found to be endemic in African countries [31].
A high diversity of clonal lineages has been identified among methicillin-susceptible S. aureus (MSSA) strains isolated from animals (livestock, domestic, and wild animals) in Africa. CC1 and CC15 were frequently detected in African countries [32]. CC80-MRSA was isolated from nasal swabs of sheep in Côte d’Ivoire, Algeria, and Tunisia [33,34,35]. S. aureus belonging to CC88-MRSA, CC5-MRSA and CC22-MRSA were also found in bovine mastitis in Egypt [36].
In Algeria, studies describing the clonal diversity of S. aureus in both, humans and animals, were limited or focused on MRSA in some regions or restricted to specific animal species. It has been reported that the clone ST80-MRSA was predominant in human isolates [15,25,37]. In these studies, isolates carried SCCmec elements of type IV, II, or V and PVL genes have been found. In livestock, few studies reported that PVL-positive ST80-MRSA-IV and ST152-MSSA were recognized in camels and sheep [35]. CC130-MSSA was mostly found in sheep and goat mastitis [38,39]. There are only a few publications about the clonal diversity of S. aureus isolated from food matrices in Algeria [40].
The aim of the present study was to investigate the clonal diversity and pathogenicity of S. aureus isolates and highlight their origins, lineages, and possible dissemination alongside the food chain. In this study, clonal lineages of MSSA and MRSA isolates collected from human and food samples in northern Algeria were characterized using DNA microarrays, and provided useful data on their virulence factor genes and antibiotic resistance-associated genes.

2. Materials and Methods

2.1. Sample Collection

The sampling procedure of this study was performed between January 2017 to January 2018 in two provinces (“wilayas”) of Médéa and Ain-Defla in northern Algeria. The provinces of Médéa and Ain Defla are two neighboring regions located in the central region of Algeria at nearly 100 km from the capital Algiers covering an area of 8866 km² and 4897 km², respectively. The two regions are characterized by a temperate Mediterranean climate. The region of Ain Defla and the north of Médéa are characterized by cereal cultivation and bovine farming. The south of Médéa belongs to an agro-pastoral region with animal breeding with a focus on sheep farming.
In this study, 71 volunteers (veterinarians and farmers) having contact with livestock animals and others with less exposure to animals such as administrative clerks were screened for staphylococcal nasal carriage. The nasal samples were obtained from both nares with sterile cotton swabs and were transported to the laboratory for microbiological examination.
Furthermore, 112 food samples (raw milk, beef meat, sausages, chicken meat, and creamery cake) were collected from several commercial vendors. The samples were cooled and transferred to the laboratory for microbiological examinations. Thirty-six S. aureus isolated from clinical samples and nasal swabs were kindly provided from local health-care facilities and private labs in the two provinces and were collected during the same time of food sampling.

2.2. Ethical Statement

The study protocol was approved by the Medical Ethics Research Committee of the Yahia Farès University, Urban Pole, Médéa, Algeria, and from the managers of the hospital in which the study was conducted. Informed written consent was obtained from each participant in the study. Confidentiality and personal privacy were respected at all levels of the study. Collected data will not be used for any other purpose.

2.3. Isolation of Staphylococcus spp.

The bacteriological analyses of samples from humans (nasal swabs, clinical samples) were performed using conventional methods, as described previously [41,42].
Nasal swabs and clinical samples were inoculated into Brain Heart Infusion (BHI) broth (Oxoid Ltd., Basingstoke, UK) and incubated overnight at 37 °C. Initial broth culture was streaked on Mannitol Salt Agar (MSA) (Oxoid Ltd., Basingstoke, UK) and Columbia agar supplemented with 5% sheep blood and incubated at 37 °C for 24 to 48 h. The plates were inspected for characteristic morphology of staphylococci and suspicious colonies were identified using conventional methods (Gram staining, catalase, and coagulase reactions) in accordance with standard microbiological methods [43]. The food samples were processed according to EN ISO 6888 1-2 1999 [44] using Baird–Parker medium supplemented with 5% of egg yolk emulsion (Oxoid Ltd., Basingstoke, UK) and 0.5% potassium tellurite. Colonies with typical shape were selected for presumptive conventional phenotypic and biochemical identification using catalase and coagulase tests.
Colonies were conserved on BHI broth with 50% of glycerol as well as by freeze-drying method in skimmed milk until further investigations.

2.4. MALDI-TOF MS Identification

Matrix-assisted laser desorption-ionization time-of-flight mass spectrometry (MALDI-TOF MS) was used for species identification; the procedure was performed as described by Bizzini and Greub, 2010 [45].
Briefly, all suspected isolates were subcultured on Mueller–Hinton agar (Oxoid Ltd., Basingstoke, UK) supplemented with 5% sheep blood at 37 °C for 24 h. Pure colonies were put in 300 μL of water, vortexed and then precipitated with 900 µL ethanol (96% vol/vol) (Carl Roth GmbH, Karlsruhe, Germany). After centrifugation for 5 min at 10,000× g, the pellet was resuspended with a volume of 50 μL of 70% (vol/vol) formic acid (Sigma Aldrich Chemie GmbH, Steinheim, Germany) and 50 μL of acetonitrile (Carl Roth GmbH, Karlsruhe, Germany). After centrifugation for 5 min at 10,000× g, 1.5 μL of the supernatant was spotted onto a MTP 384 Target Plate Polished Steel TF (Bruker Daltonik GmbH, Bremen, Germany) and allowed to air dry at room temperature. A droplet of 2 μL of matrix solution (α-cyano-4-hydroxycinnamic acid) (Sigma-Aldrich Chemie GmbH, Taufkirchen, Germany) was added on top of each sample spot and again the spots were completely dried. Spectra recording was performed using an Ultraflex instrument (Bruker Daltonik GmbH, Bremen, Germany) and data were automatically analyzed using the Biotyper 3.1 software (Bruker Daltonik, Bremen, Germany).

2.5. Molecular Identification of Staphylococcus spp.

DNA was extracted from suspected Staphylococcus colonies using the HighPure PCR Template Preparation Kit (Roche Diagnostics Deutschland GmbH, Mannheim, Germany) according to the manufacturer’s instructions. DNA quantity and purity were determined using a NanoDrop™ 1000 spectrophotometer (Thermo Fisher Scientific, Wilmington, MA, USA).
A multiplex real-time PCR assay was performed to detect 16S rRNA, nuc and mecA genes corresponding to Staphylococcus spp., S. aureus, and MRSA, respectively [46]. The multiplex real-time PCR TaqMan assay was carried out with the LightCycler 480 Probes Master kits (Roche Diagnostic Deutschland GmbH, Mannheim, Germany) using the CFX-96 real-time PCR system (Bio-Rad, Hercules, CA, USA), which was used for thermocycling and fluorescence detection as described previously [46]. The real-time PCR amplification was performed in a total volume of 25 μL containing 10 μL of PCR master-mix (1×), 6.75 μL of primers (0.2 µM) and TaqMan probe (0.1 µM) mixture and 5 μL of template DNA (100 pg/µL); distilled water was added for a final volume of 25 μL.

2.6. DNA Microarray Analysis

The microarray carried 334 oligonucleotide probes for virulence-associated genes including genes encoding exotoxins and enterotoxins, immune evasion factors, microbial surface components recognizing adhesive matrix molecules (MSCRAMM) as well as resistance determinants and other target genes for typing markers such as species, SCCmec, capsule, and agr group typing markers. DNA microarray analysis was performed on the ArrayStrip platform using the S. aureus specific DNA microarray assay (StaphyType; Abbott (Alere Technologies GmbH), Jena, Germany) following the manufacturer’s instructions. Briefly, bacterial colonies were picked from an overnight culture on blood agar. The genomic DNA was extracted after bacterial cells lysis using the EZ1 system (Qiagen, Hilden, Düsseldorf, Germany). Purified nucleic acids were subjected to a linear primer elongation. Biotin-16-dUTP was integrated into the resulting amplicons. Labeled genomic DNA was hybridized to the probes of the microarray. After washing, horseradish-peroxidase-streptavidin conjugate was added followed by precipitation with a special dye. Then, a scanned image was obtained by a microarray reader and subsequently the data were analyzed automatically using software provided by Alere Technologies GmbH. According to difference in the intensity of the colors for each spot, results interpretation was done as “positive” (present), “negative” (absent) or “ambiguous” as described previously [10,47,48].
The clonal complex recognition was based on analysis of hybridisation profiles with regard to non-motile genes, as previously reported [49].

3. Results

In this study, 60 S. aureus were isolated and identified using MALDI-TOF MS and real-time PCR. Twenty-four strains were isolated from 112 food samples, 16 were isolated from 71 nasal swabs and 20 clinical strains were kindly provided from hospital and private labs collection. The origin and distribution of S. aureus are shown in Table 1.
Twenty-four S. aureus isolated from food samples were predominantly isolated from raw milk (10 isolates), minced beef meat (10 isolates), creamy cake (2 isolates), chicken meat (one isolate) and sausages (one isolate) (Table 1).
Staphylococcus aureus isolated in this study were grouped into 14 different clonal complexes using DNA microarray analysis (Table 1; Figure 1 and Table S1). Out of 24 S. aureus isolated from food, 6 different CCs were identified, while 9 different CCs were determined for 20 clinical isolates and those of nasal swabs (Table 1).
Seventeen (28.3%) out of 60 S. aureus isolates were identified as MRSA and they were mainly found in clinical isolates (10/17 (58.8%)). Only a minority was detected in food samples (3/17 (17.6%) and nasal samples (4/17 (23.5%)).
Regardless of their origin, 13 (21.7%) and 10 (16.7%) out of 60 S. aureus isolates belonged to CC1-MSSA and CC97-MSSA, respectively. These two CC were the most common clonal complexes.
The clinical isolates mainly belonged to CC80-MRSA (6/20 (30%)), followed by the CC1-MSSA and CC6-MRSA (3 /20 (15%) for each).
Ten (41.7%) and eight (33.3%) of 24 S. aureus isolated from food clustered mainly within CC1-MSSA and CC97-MSSA, respectively.
The occurrence of virulence-associated factors as detected by microarray analysis is summarized in Table 2 and Table 3.
Out of 60 S. aureus, 27 (45%) possessed the accessory gene regulator allele agr group III with a predominance of clinical isolates (19/27; 70.4%). Isolates having agr-III alleles belonged to CC1-MSSA, CC80-MRSA, CC30-MSSA, and CC5-MSSA (Table 2). The agr-I was detected in CC6-MRSA, CC22-MSSA, CC22-MRSA, CC45-MSSA, CC97-MSSA and CC398-MSSA. The agr group II alleles were found in isolates assigned to CC15-MSSA, CC479- MSSA and CC705-MSSA.
Panton-Valentine leukocidin genes lukF/lukS-PV were detected in 8 (13.3%) CC80 MRSA, which mainly originated from pus samples (4 isolates), urine and catheter (one isolate for each) of human origin. The genes lukF-PV (P83) and lukM were present in two isolates belonging to CC479-MSSA and CC705-MSSA. However, lukF, lukS, hlgA and hla encoding for hemolysins and leukocidin components were detected in all S. aureus isolates. The capsule type 5 gene cluster cap5 was carried by 24 (40%) isolates mainly belonging to CC5-MSSA, CC22-MSSA, CC22-MRSA and CC97-MSSA. Contrary, the cap8 gene cluster was harbored by 36 (60%) isolates mainly belonging to CC1-MSSA (13 isolates) and CC80-MRSA (8 isolates).
The ica operon ACD responsible for intercellular adhesion protein AB and biofilm PIA synthesis protein D was detected in all isolates, whereas the bap gene encoding surface protein involved in biofilm formation was found only in one CC15-MSSA isolate recovered from a pus sample of a patient with a hospital-acquired infection.
The gene encoding for toxic shock syndrome toxin 1 (tst1) was found in 8 human isolates assigned to CC22-MSSA and CC22-MRSA. Genes etA/B encoding for exfoliative toxins were not detected, while the etD gene was present in all CC80-MRSA isolates. The edinB gene encoding for epidermal cell differentiation inhibitor B was likewise detected in all isolates belonging to CC80-MRSA whereas, edinA and edinC genes were not detected.
Genes encoding for enterotoxins were detected in several isolates: The sea gene was found in 17 isolates (10 human isolates and 7 food isolates) belonging to CC1-MSSA, CC5-MSSA, CC6-MRSA, CC8-MSSA and CC30-MSSA. The seb and sec genes were identified in 5 and 2 isolates, respectively. The enterotoxin gene cluster egc was present in 17 isolates. The clinical isolates carrying the sea gene were predominantly collected from samples of community infections and the food isolates harboring this gene originated from milk and minced beef meat.
In all isolates we detected adhesion factors and genes encoding MSCRAMM [bone binding protein (bbp), clumping factors (clfA/B), collagen-binding adhesion (cna), cell wall-associated fibronectin-binding protein (ebh), cell surface elastin-binding protein (ebpS), enolase (eno), fibrinogen-binding protein (fib), fibronectin-binding protein A (fnbA), major histocompatibility complex class II (extracellular adherence protein), extracellular adherence protein (map), S. aureus surface protein G (sasG) and fibrinogen-/bone sialoprotein-binding protein C/D (sdrC/D) and van Willebrand factor-binding protein (vwb)] were detected in all isolates.
The genes responsible for antimicrobial resistance detected by microarray analysis are shown in Table 4.
The antibiotic resistance gene carriage was observed in different isolates regardless their origin.
Seventeen (28.3%) S. aureus isolates carried the mecA gene localized on SCCmec type IV elements. These isolates were identified as methicillin-resistant. The remaining S. aureus isolates (43/60; 71.7%) were methicillin-susceptible. The 17 MRSA isolates belonged to three different CCs (CC6, CC80, and CC22) and mainly originated from clinical samples (7 community-acquired MRSA and 3 hospital-acquired MRSA), 3 MRSA isolates from food, and 4 MRSA isolates came from nasal swabs.
Genes encoding for antibiotic resistance to β-lactamase (blaZ/I/R) were found in 71.7% (43/60) of isolates.
The erm(C) gene encoding for macrolide/clindamycin resistance was found in seven MRSA isolates, while only two MSSA isolates (food samples) assigned to CC97 carried the erm(B) gene.
Fusidic acid resistance gene fusC was detected in all CC1 isolates. The tetK gene associated with tetracycline resistance was identified in 15 S. aureus isolates (7 food and 8 clinical isolates). In one food isolate belonging to CC1-MSSA, tetK and tetM were detected simultaneously.
Additionally, the aadD gene, which is responsible for tobramycin resistance, was detected in one clinical isolate.
In addition to mecA gene carriage, clinical isolates that belonged to CC80-MRSA harbored antimicrobial resistance genes blaZ, ermC, aphA3, sat, far1 and tetK. They were recovered from pus samples (4 isolates), urine (1 isolate) and a catheter (1 isolate). CC97-MSSA isolated from food samples carried several antibiotic resistance genes (blaZ, ermB, aphA3, sat, tetM, and tetK genes). These strains were mainly isolated from milk samples (n = 5), cream cake (n = 2) and minced beef meat (n = 1) (Table 1).

4. Discussion

To estimate the potential health hazards caused by S. aureus transmission, it is imperative to study their origins, lineages and dissemination simultaneously on humans, in the environment, on animal farms and alongside the food chain.
The present study was aimed to provide relevant information (clonal complex lineages, agr types, virulence and antimicrobial resistance-associated genes) about S. aureus isolated from a variety of human clinical, nasal and food samples in northern Algeria based on DNA microarray assay. This study focused only on two provinces (Médéa and Ain-Defla) in Algeria and hence our results cannot be generalized for a larger scale.
In this study, 24 S. aureus from food sources originated predominantly from raw milk and minced beef meat and only three of them were identified as MRSA. These findings corroborated several studies reporting low percentages of MRSA in food samples [51,52,53].
The majority of clinical isolates of S. aureus were recovered from pus and suppurative infections in which 50% were identified as MRSA (7 CA-MRSA and 3 HA-MRSA). It is known that S. aureus isolates are considered as a principal pathogenic agent in skin and soft tissue infections [54].
Out of 16 S. aureus isolated from nasal carriage from individuals with contact to livestock animals, four (25%) were identified as MRSA. These findings were lower compared to previous reports conducted in Algeria on resembled populations [35,55].
Molecular genotyping of isolated S. aureus resulted in assignment to a high variety of CCs. The general trend showed that CCs in clinical or food samples were closely similar, in contrast to those detected in nasal carriage. The lineages found in food isolates mostly belonged to CC1-MSSA and CC97-MSSA. The majority of CC97 (62.5%) originated from milk samples. Previous studies indicated that S. aureus isolated from bovine milk belonged to CC97 and were mainly represented by isolates from ruminants [9,10,20,56,57]. CC97 strains are occasionally isolated from humans [58] and rarely found as MRSA [59].
Two human isolates belonged to the common bovine lineage CC97, suggesting a possible jump from cattle to humans, as reported previously [60]. A previous work carried out in the same region as the present study indicated that CC97 is associated with bovine subclinical mastitis [55], suggesting a possible origin of these milk samples from infected udders without rigorous surveillance.
The majority of CC1-MSSA isolates originated from meat samples and the remaining came from milk samples which in agreement with a previous study conducted by Wu et al., 2018 reported that most of S. aureus isolated from retail meat and meat products belonged to CC1-MSSA [61]. The CC1-MSSA is thought to be of human origin and began to emerge within bovine S. aureus populations causing mastitis [62], which could subsequently contaminate milk, as previously reported [9].
In this study, three MRSA belonging to CC6-MRSA-IV and CC80-MRSA-IV were isolated from food samples (minced beef meat). These lineages are likely to be found in human samples [25,63] so that this observation might indicate a possible contamination by humans at the slaughterhouse or during processing [64]. Another study showed that commercially distributed meat could play a role in the spreading of CA-MRSA [65]. However, there is no evidence that the transmission of such lineages (lacking enterotoxin genes) would increase the risk of foodborne infections [66].
Six MRSA strains isolated from clinical samples belonged to CC80-MRSA-IV. They were PVL positive and carried SCCmec type IV. This lineage has previously been found in clinical samples in Algeria [15,25,37,67], Tunisia [68], Egypt [16], Europe [23], North America [18], the Middle East [69] and Australia [19]. The results suggest that this clonal complex is a highly prevalent MRSA lineage that has already spread across the North African countries, Egypt and the Middle East and that also can be found sporadically beyond that region.
Seven of the clinical MSSA strains were assigned to CC1, CC5, and CC15 which in agreement with previously reported diversity of CCs in MSSA isolated from patients with infected diabetic foot ulcer in which MSSA isolates belonged to CC1 and CC15 [37].
Staphylococcus aureus from nasal swabs essentially belonging to CC22 (CC22-MSSA and CC22-MRSA); only one isolate belonged to CC80-MRSA IV. The results coincide with previous report, which found that MRSA in nasal carriers on farms belonged to CC22-MRSA-IV and CC80-MRSA-IV [55]. The prominent epidemic CC22 lineage is known as a typical widespread human-associated clone, and there are several distinct MRSA strains that are responsible for both, hospital-acquired and community-acquired MRSA infections [59,70].
One nasal carriage isolate was assigned to CC398-MSSA. The results of a former study strongly suggested that LA-MRSA CC398 originated in humans as MSSA [71]. This clone has been recovered also from food of animal origin [72]. Staphylococcus aureus of ST398 is known to have comparable low host specificity and is able to colonize or cause infections in a broad variety of animal species, including humans [59,73]. It is worth to note that isolated CC398-MSSA lacked many virulence factors such as the Panton–Valentine leukocidin toxin or enterotoxin genes; also, no antibiotic resistance determinants were detected. In fact, the transmission of some clones from animals to humans and vice versa is accompanied by the acquisition of adaptation factors and at the same time loss of certain virulence factors [73,74].
The present findings on human nasal carriage revealed that one S. aureus belonged to CC705-MSSA. It was reported that this clone was not of human origin but it is a common lineage in cattle [60,75]. In the same way, Agabou et al., 2017 found only two CC705-MSSA isolates in Algerian cattle nasal carriage without any detection of this clone in noses of farm workers [35]. Furthermore, it was reported that CC705 (ST705) has emerged as a dominant lineage derived from bovine milk worldwide [56]. Thus, we assume a transmission from an animal or food source to the human carrier.
Two isolates originating from nasal carriage were assigned to CC15-MSSA. Monecke et al. (2009) reported that CC15-MSSA are mainly isolated from healthy carriers [76]. In addition, it was suggested that MRSA from this lineage are extremely rare [59]. Two other human isolates assigned to CC30-MSSA were identified in this study. A previous study showed that CC30 is an important clonal complex from which virulent MSSA as well as HA and CA-MRSA originated [59].
In the present study, other S. aureus lineages, such as CC30 and CC45, were recovered from nasal carriers. These CCs were described in the past among other clusters of strains colonizing healthy individuals in Europe [73,76,77].
In this study, Panton–Valentine leukocidin genes lukF/lukS-PV were detected in 8 S. aureus isolated from clinical samples and belonging to CC80-MRSA. In concordance, a study described that all MRSA harboring lukF/lukS-PV belonged to CC80 [37]. Other reports confirming that PVL gene carriage associated with CC80 is widely distributed in North African countries, including Algeria [15,25].
From the three MRSA isolated from food samples, we found only one PVL-positive. Recently, Mairi et al., 2019 found also some MRSA-PVL positive isolates from food belonging to the ST80-IV CA-MRSA clone [52]. However, MRSA PVL-positive clonal lineages are rare in milk products [78] or in animals [35,79].
The leukocidin genes lukF-PV(P83) (F component from hypothetical leukocidin of ruminants) and lukM were detected in CC705 (nasal carriage isolate) and CC479 (food isolate). Schlotter et al., 2012, found that the majority of CC479 S. aureus isolates from milk of dairy herds harbored the leukocidin genes lukF-(P83)/lukM [80]. In a comparative study of 456 strains of S. aureus isolated from milk of bovine intramammary infections and bulk tanks obtained from 12 European countries, it was reported that isolates were predominantly assigned to CC705 [81]. In addition, several studies reported that CC705 is a common bovine clone among bovine mastitis S. aureus isolates [55,60,82] and from nasal carriage in cattle [35]. The detection of leukocidin genes lukF-PV (P83)/lukM in a human nasal swab isolate CC705 suggests zoonotic transmission from bovine to humans in close contacts.
In this study, sea and seh genes were notably detected in CC1 MSSA isolated from food samples. Staphylococcal food poisoning (SFP) is an intoxication caused by ingestion of contaminated foods (milk, cream filled pastries, sandwich filling, sausages, ground meat, salads, and cooked meals) containing sufficient quantity of staphylococcal enterotoxins (SEs). The most important enterotoxins involved in SFP are the classical SEA, and the SEH [3]. Monecke et al., 2011 found that all CC1-MRSA isolates harbored the enterotoxin gene seh [59]. Others found the seh gene in S. aureus isolates from milk and milk products [78]. Also, Jørgensen et al., 2005 reported that SEH was responsible for milk-associated food-poisoning outbreaks [83].
It has been reported that isolates harboring the gene encoding for toxic shock syndrome toxin 1 (tst1) in combination with other toxin genes were highly pathogenic for humans [84]. In this study, isolates possessing the tst1 gene were negative for lukFS-PV, lukF-PV (P83), luk-M, sea, seb and sec genes.
Biofilm formation is regulated by expression of polysaccharide intracellular adhesion (PIA) protein, which mediates cell-to-cell adhesion and is the product of the ica locus containing icaA/B/C/D [85]. The operon icaACD was detected in all isolates. The bap gene encoding surface protein involved in biofilm formation was found only in one CC15-MSSA isolate. All MRSA SCCmec type IV isolates possessed the icaACD genes responsible for biofilm formation and carried the MSCRAMMs genes. In concordance, Mirani et al., 2013 found that 98.3% of foodborne MRSA isolates carried the icaA/SCCmec IV profile [86], while an association of SCCmec type V and icaA gene was also reported [87,88].
The present study showed a high rate of MRSA in clinical samples (50%). The national rate in Algeria was approximately 35% for hospitalized patients (www.sante.dz/aarn/documents/pdf/rapport16.pdf, accessed on 27 September 2021). Several Algerian studies focusing on human isolates showed that the MRSA rate has increased almost tenfold in just two decades from less than 5% in 1996–1997 [89] to 50% in 2011 [25] and 62.2% in 2014 [90].
In this study, all MRSA isolates carried the SCCmec IV type. Previous Algerian studies reported that MRSA strains mostly harbored the SCCmec IV type [15,25,67,91]. Additionally, others SCCmec types were found at lower rates: 43.75% of MRSA carried SCCmec V type [91]. SCCmec II in one isolate [15], SCCmec type III [25,67], while Alioua et al. (2014) found more SCCmec type III compared to SCCmec type IV [90].
Resistance to antibiotics can result from the imprudent use of antimicrobial agents in human and animals. In this study, 71.7% of all S. aureus and 88.2% of MRSA isolates carried the penicillinase operon blaZ. Previous Algerian studies reported penicillin resistance in 96 to 100% of clinical isolates [92] and in nasal human carriage, 91.6% of isolates carried the blaZ gene [35].
The detection of genes encoding resistance towards tetracycline (tetM and tetK) was not surprising, as this broad-spectrum antibiotic is widely used by Algerian veterinarians and farmers [93]. A resistance rate as high as 85% to tetracycline among MRSA strains isolated from poultry was recently reported [94]. In addition, tetracycline resistance could be expected in other bacterial genera as a consequence of the extensive use of tetracycline in livestock [93].
The putative/questionable fosfomycin resistance gene fosB was described by Djahmi et al., 2013, who found a high rate of clinical isolates assigned to several CCs (ST239-MRSA, ST80-MRSA, CC1-, CC15-, CC121-, CC9-, CC54- and ST152-MSSA) harboring fosB [37]. Indeed, it was reported to be specific for certain clonal complexes such as CC5, CC8, CC12, CC15, CC20, CC25, CC30 and S. argenteus ST1850 [49].
Monecke et al., 2011 found that nearly all CC80-MRSA-IV isolates carried the aphA3 and sat and plasmid harbored genes blaZ, tetK and far1. Additional resistance genes ermC were rarely detected [59]. In concordance, all CC80-MRSA-IV isolated in this study harbored the aphA3 and sat genes. 87.5% carried the genes far1, tetK and blaZ and 25% carried the ermC gene. Others reports showed also that MRSA-ST80 isolates can be resistant to fusidic acid, tetracycline and kanamycin [95,96]. Ultimately, we considered CC80-MRSA-IV isolates of the present study as multidrug-resistant.

5. Conclusions

The DNA microarray results obtained in this study showed that CC 80-MRSA- IV is a significant pathogen among clinical isolates. This clone was found to be associated with many virulence factors (lukF/lukS-PV, edinB and sea) and antibiotics resistance genes (sat, aphA3, far1, tetK and blaZ). In addition, food isolates mostly assigned to CC1 and CC97 were found to harbor enterotoxins genes and antibiotic resistance genes. It was also observed that almost all clones were found in their typical host, but interestingly, some nasal carriers had isolates assigned to CC705 thought to be absent in humans. Our data suggest a possible jump from animals to humans and constitute a dissemination risk into the community. Staphylococcus aureus continues to be a serious human health challenge and the detection of MRSA strains among food isolates should be considered as a potential public health risk. It is necessary to monitor the health status of animals and improve hygiene conditions in the food chain to limit the dissemination of pathogenic and multidrug-resistant strains. Therefore, it is crucial to revise antibiotic prescriptions for rational use in human and animal infections.

Supplementary Materials

The following are available online at https://www.mdpi.com/article/10.3390/pathogens10101276/s1, Table S1: The results of Microarray assay analysis for 60 S. aureus.

Author Contributions

Data curation, R.A., I.N. and T.M.H.; methodology, R.A., H.E.-A., I.N., H.H., R.E. and S.M.; investigation, R.A., I.N., A.H. and T.M.H.; writing—original draft preparation, R.A., I.N., H.H. and H.E.-A.; writing—review and editing, H.H., T.M.H., R.E., S.M., A.H., H.N., H.T. and H.E.-A.; supervision, H.H., H.T., H.E.-A. and H.N. All authors have read and agreed to the published version of the manuscript.

Funding

ADA (13GW0456C: BMBF): Adaptable decentralized diagnostics for veterinary and human medicine.

Institutional Review Board Statement

The study was conducted according to the guidelines of the Declaration of Helsinki, and approved by the Institutional Review Board of the Medical Ethics Research Committee of the Yahia Farès University, Urban Pole, Médéa, Algeria, (protocol code 068/LCEPC/2017 at 08.02.2017) and from the managers of the hospital in which the study was conducted.

Informed Consent Statement

Informed consent was obtained from all subjects involved in the study.

Data Availability Statement

The data presented in this study are available on request from the corresponding author.

Acknowledgments

The authors thank Byrgit Hofmann and Peggy Methner at the Institute of Bacterial Infections and Zoonoses, Friedrich-Loeffler-Institut, Jena, Germany, and Elke Müller and Annett Reissig at the Leibniz Institute of Photonic Technology (IPHT), Jena, Germany, for their excellent technical assistance. The authors thank Faiza Mebkhout for the help with nasal swab samples collection.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Lindsay, J.A.; Holden, M.T. Understanding the rise of the superbug: Investigation of the evolution and genomic variation of Staphylococcus aureus. Funct Integr Genom. 2006, 6, 186–201. [Google Scholar] [CrossRef] [PubMed]
  2. Tristan, A.; Rasigade, J.P.; Ruizendaal, E.; Laurent, F.; Bes, M.; Meugnier, H.; Lina, G.; Etienne, J.; Celard, M.; Tattevin, P.; et al. Rise of CC398 lineage of Staphylococcus aureus among Infective endocarditis isolates revealed by two consecutive population-based studies in France. PLoS ONE 2012, 7, 13. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  3. Le Loir, Y.; Baron, F.; Gautier, M. Staphylococcus aureus and food poisoning. Genet. Mol. Res. 2003, 2, 63–76. [Google Scholar]
  4. Foster, T.J.; Geoghegan, J.A.; Ganesh, V.K.; Hook, M. Adhesion, invasion and evasion: The many functions of the surface proteins of Staphylococcus aureus. Nat. Rev. Microbiol. 2014, 12, 49–62. [Google Scholar] [CrossRef] [Green Version]
  5. Otto, M. Staphylococcus aureus toxins. Curr Opin Microbiol. 2014, 17, 32–37. [Google Scholar] [CrossRef] [Green Version]
  6. Palavecino, E.L. Clinical, epidemiologic, and laboratory aspects of methicillin-resistant Staphylococcus aureus infections. Methods Mol. Biol. 2014, 661–664. [Google Scholar]
  7. Bosch, T.; Pluister, G.N.; van Luit, M.; Landman, F.; van Santen-Verheuvel, M.; Schot, C.; Witteveen, S.; van der Zwaluw, K.; Heck, M.E.; Schouls, L.M. Multiple-locus variable number tandem repeat analysis is superior to spa typing and sufficient to characterize MRSA for surveillance purposes. Future Microbiol. 2015, 10, 1155–1162. [Google Scholar] [CrossRef]
  8. El-Adawy, H.; Ahmed, M.; Hotzel, H.; Monecke, S.; Schulz, J.; Hartung, J.; Ehricht, R.; Neubauer, H.; Hafez, H.M. Characterization of methicillin-resistant Staphylococcus aureus isolated from healthy turkeys and broilers using DNA microarrays. Front. Microbiol. 2016, 7. [Google Scholar] [CrossRef]
  9. McMillan, K.; Moore, S.C.; McAuley, C.M.; Fegan, N.; Fox, E.M. Characterization of Staphylococcus aureus isolates from raw milk sources in Victoria, Australia. BMC Microbiol. 2016, 16, 169. [Google Scholar] [CrossRef] [Green Version]
  10. Monecke, S.; Kuhnert, P.; Hotzel, H.; Slickers, P.; Ehricht, R. Microarray based study on virulence-associated genes and resistance determinants of Staphylococcus aureus isolates from cattle. Vet. Microbiol. 2007, 125, 128–140. [Google Scholar] [CrossRef] [PubMed]
  11. Stefani, S.; Chung, D.R.; Lindsay, J.A.; Friedrich, A.W.; Kearns, A.M.; Westh, H.; Mackenzie, F.M. Meticillin-resistant Staphylococcus aureus (MRSA): Global epidemiology and harmonisation of typing methods. Int J. Antimicrob Agents. 2012, 39, 273–282. [Google Scholar] [CrossRef] [PubMed]
  12. Chatterjee, S.S.; Otto, M. Improved understanding of factors driving methicillin-resistant Staphylococcus aureus epidemic waves. Clin. Epidemiol. 2013, 5, 205–217. [Google Scholar] [PubMed] [Green Version]
  13. Armand-Lefevre, L.; Ruimy, R.; Andremont, A. Clonal comparison of Staphylococcus aureus isolates from healthy pig farmers, human controls, and pigs. Emerg Infect. Dis. 2005, 11, 711–714. [Google Scholar] [CrossRef]
  14. Smith, T.C.; Pearson, N. The emergence of Staphylococcus aureus ST398. Vector Borne Zoonotic Dis. 2011, 11, 327–339. [Google Scholar] [CrossRef]
  15. Djoudi, F.; Bonura, C.; Benallaoua, S.; Touati, A.; Touati, D.; Aleo, A.; Cala, C.; Fasciana, T.; Mammina, C. Panton-Valentine leukocidin positive sequence type 80 methicillin-resistant Staphylococcus aureus carrying a staphylococcal cassette chromosome mec type IVc is dominant in neonates and children in an Algiers hospital. New Microbiol. 2013, 36, 49–55. [Google Scholar] [PubMed]
  16. Enany, S.; Yaoita, E.; Yoshida, Y.; Enany, M.; Yamamoto, T. Molecular characterization of Panton-Valentine leukocidin-positive community-acquired methicillin-resistant Staphylococcus aureus isolates in Egypt. Microbiol Res. 2010, 165, 152–162. [Google Scholar] [CrossRef]
  17. Mariem, B.J.; Ito, T.; Zhang, M.; Jin, J.; Li, S.; Ilhem, B.B.; Adnan, H.; Han, X.; Hiramatsu, K. Molecular characterization of methicillin-resistant Panton-valentine leukocidin positive Staphylococcus aureus clones disseminating in Tunisian hospitals and in the community. BMC Microbiol. 2013, 13, 1471–2180. [Google Scholar] [CrossRef] [Green Version]
  18. Tenover, F.C.; McDougal, L.K.; Goering, R.V.; Killgore, G.; Projan, S.J.; Patel, J.B.; Dunman, P.M. Characterization of a strain of community-associated methicillin-resistant Staphylococcus aureus widely disseminated in the United States. J. Clin. Microbiol. 2006, 44, 108–118. [Google Scholar] [CrossRef] [Green Version]
  19. Coombs, G.W.; Goering, R.V.; Chua, K.Y.L.; Monecke, S.; Howden, B.P.; Stinear, T.P.; Ehricht, R.; O’Brien, F.G.; Christiansen, K.J. The molecular epidemiology of the highly virulent ST93 Australian community Staphylococcus aureus strain. PLoS ONE 2012, 7, e43037. [Google Scholar] [CrossRef] [Green Version]
  20. Cuny, C.; Friedrich, A.; Kozytska, S.; Layer, F.; Nubel, U.; Ohlsen, K.; Strommenger, B.; Walther, B.; Wieler, L.; Witte, W. Emergence of methicillin-resistant Staphylococcus aureus (MRSA) in different animal species. Int J. Med. Microbiol. 2010, 300, 109–117. [Google Scholar] [CrossRef]
  21. Sung, J.M.; Lloyd, D.H.; Lindsay, J.A. Staphylococcus aureus host specificity: Comparative genomics of human versus animal isolates by multi-strain microarray. Microbiol. 2008, 154, 1949–1959. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  22. Voss, A.; Loeffen, F.; Bakker, J.; Klaassen, C.; Wulf, M. Methicillin-resistant Staphylococcus aureus in pig farming. Emerg Infect. Dis. 2005, 11, 1965–1966. [Google Scholar] [CrossRef] [PubMed]
  23. Vandenesch, F.; Naimi, T.; Enright, M.C.; Lina, G.; Nimmo, G.R.; Heffernan, H.; Liassine, N.; Bes, M.; Greenland, T.; Reverdy, M.E.; et al. Community-acquired methicillin-resistant Staphylococcus aureus carrying Panton-Valentine leukocidin genes: Worldwide emergence. Emerg Infect. Dis. 2003, 9, 978–984. [Google Scholar] [CrossRef] [PubMed]
  24. Miller, L.G.; Perdreau-Remington, F.; Rieg, G.; Mehdi, S.; Perlroth, J.; Bayer, A.S.; Tang, A.W.; Phung, T.O.; Spellberg, B. Necrotizing fasciitis caused by community-associated methicillin-resistant Staphylococcus aureus in Los Angeles. N Engl J. Med. 2005, 352, 1445–1453. [Google Scholar] [CrossRef] [Green Version]
  25. Antri, K.; Rouzic, N.; Dauwalder, O.; Boubekri, I.; Bes, M.; Lina, G.; Vandenesch, F.; Tazir, M.; Ramdani-Bouguessa, N.; Etienne, J. High prevalence of methicillin-resistant Staphylococcus aureus clone ST80-IV in hospital and community settings in Algiers. Clin. Microbiol Infect. 2011, 17, 526–532. [Google Scholar] [CrossRef] [Green Version]
  26. Wangai, F.K.; Masika, M.M.; Maritim, M.C.; Seaton, R.A. Methicillin-resistant Staphylococcus aureus (MRSA) in East Africa: Red alert or red herring? BMC Infect. Dis. 2019, 19, 596. [Google Scholar] [CrossRef]
  27. Conceição, T.; Santos Silva, I.; de Lencastre, H.; Aires-de-Sousa, M. Staphylococcus aureus nasal carriage among patients and health care workers in São Tomé and Príncipe. Microb Drug Resist. 2014, 20, 57–66. [Google Scholar] [CrossRef]
  28. Egyir, B.; Guardabassi, L.; Sørum, M.; Nielsen, S.S.; Kolekang, A.; Frimpong, E.; Addo, K.K.; Newman, M.J.; Larsen, A.R. Molecular epidemiology and antimicrobial susceptibility of clinical Staphylococcus aureus from healthcare institutions in Ghana. PloS one. 2014, 9, e89716. [Google Scholar] [CrossRef] [Green Version]
  29. Shittu, A.O.; Oyedara, O.; Abegunrin, F.; Okon, K.; Raji, A.; Taiwo, S.; Ogunsola, F.; Onyedibe, K.; Elisha, G. Characterization of methicillin-susceptible and -resistant staphylococci in the clinical setting: A multicentre study in Nigeria. BMC Infect. Dis. 2012, 12, 286. [Google Scholar] [CrossRef] [Green Version]
  30. Oosthuysen, W.F.; Orth, H.; Lombard, C.; Sinha, B.; Wasserman, E. In vitro characterization of representative clinical South African Staphylococcus aureus isolates from various clonal lineages. New Microbe New Infect. 2014, 2, 115–122. [Google Scholar] [CrossRef] [Green Version]
  31. Abdulgader, S.M.; Shittu, A.O.; Nicol, M.P.; Kaba, M. Molecular epidemiology of methicillin-resistant Staphylococcus aureus in Africa: A systematic review. Front. Microbiol. 2015, 6. [Google Scholar] [CrossRef] [PubMed]
  32. Lozano, C.; Gharsa, H.; Ben Slama, K.; Zarazaga, M.; Torres, C. Staphylococcus aureus in animals and food: Methicillin resistance, prevalence and population structure. A Review in the African Continent. Microorganisms. 2016, 4, 12. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  33. Gharsa, H.; Ben Slama, K.; Lozano, C.; Gómez-Sanz, E.; Klibi, N.; Ben Sallem, R.; Gómez, P.; Zarazaga, M.; Boudabous, A.; Torres, C. Prevalence, antibiotic resistance, virulence traits and genetic lineages of Staphylococcus aureus in healthy sheep in Tunisia. Vet. Microbiol. 2012, 156, 367–373. [Google Scholar] [CrossRef] [PubMed]
  34. Schaumburg, F.; Pauly, M.; Anoh, E.; Mossoun, A.; Wiersma, L.; Schubert, G.; Flammen, A.; Alabi, A.S.; Muyembe-Tamfum, J.J.; Grobusch, M.P.; et al. Staphylococcus aureus complex from animals and humans in three remote African regions. Clin. Microbiol Infect. 2015, 21, 11. [Google Scholar] [CrossRef] [Green Version]
  35. Agabou, A.; Ouchenane, Z.; Ngba Essebe, C.; Khemissi, S.; Chehboub, M.T.E.; Chehboub, I.B.; Sotto, A.; Dunyach-Remy, C.; Lavigne, J.P. Emergence of nasal carriage of ST80 and ST152 PVL+ Staphylococcus aureus isolates from livestock in Algeria. Toxins. 2017, 9, 303. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  36. El-Ashker, M.; Gwida, M.; Tomaso, H.; Monecke, S.; Ehricht, R.; El-Gohary, F.; Hotzel, H. Staphylococci in cattle and buffaloes with mastitis in Dakahlia Governorate, Egypt. J. Dairy Sci. 2015, 98, 7450–7459. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  37. Djahmi, N.; Messad, N.; Nedjai, S.; Moussaoui, A.; Mazouz, D.; Richard, J.L.; Sotto, A.; Lavigne, J.P. Molecular epidemiology of Staphylococcus aureus strains isolated from inpatients with infected diabetic foot ulcers in an Algerian University Hospital. Clin. Microbiol Infect. 2013, 19, E369–E404. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  38. Achek, R.; El-Adawy, H.; Hotzel, H.; Tomaso, H.; Ehricht, R.; Hamdi, T.M.; Azzi, O.; Monecke, S. Short communication: Diversity of staphylococci isolated from sheep mastitis in northern Algeria. J. Dairy Sci. 2020, 103, 890–897. [Google Scholar] [CrossRef] [Green Version]
  39. Akkou, M.; Bentayeb, L.; Ferdji, K.; Medrouh, B.; Bachtarzi, M.A.; Ziane, H.; Kaidi, R.; Tazir, M. Phenotypic characterization of staphylococci causing mastitis in goats and microarray-based genotyping of Staphylococcus aureus isolates. Small Ruminant Res. 2018, 169, 29–33. [Google Scholar] [CrossRef]
  40. Titouche, Y.; Hakem, A.; Houali, K.; Meheut, T.; Vingadassalon, N.; Ruiz-Ripa, L.; Salmi, D.; Chergui, A.; Chenouf, N.; Hennekinne, J.A.; et al. Emergence of methicillin-resistant Staphylococcus aureus (MRSA) ST8 in raw milk and traditional dairy products in the Tizi Ouzou area of Algeria. J. Dairy Sci. 2019, 102, 6876–6884. [Google Scholar] [CrossRef]
  41. Denis, F.; Ploy, M.C.; Martin, C.; Bingen, E.; Quentin, R. Bactériologie Médicale: Techniques Usuelles, 3rd ed.; Elsevier Masson SAS: Issy-les-Moulineaux, France, 2011. [Google Scholar]
  42. Oliver, S.P.; Gonzalez, R.N.; Hogan, J.S.; Jayarao, M.; Owens, W.E. Microbiological Procedures for the Diagnosis of Bovine Udder Infection and Determination of Milk Quality, 4th ed.; Council, N.M., Ed.; National Mastitis Council NMC Inc.: Verona, MN, USA, 2004. [Google Scholar]
  43. Karmakar, A.; Dua, P.; Ghosh, C. Biochemical and molecular analysis of Staphylococcus aureus clinical isolates from hospitalized patients. Can. J. Infect. Dis Med. Microbiol. 2016, 9041636, 24. [Google Scholar]
  44. ISO. Microbiology of food and animal feeding stuffs — Horizontal method for the enumeration of coagulase-positive staphylococci (Staphylococcus aureus and other species) — Part 1: Technique using Baird-Parker agar medium; ISO: Geneva, Switzerland, 2003. [Google Scholar]
  45. Bizzini, A.; Greub, G. Matrix-assisted laser desorption ionization time-of-flight mass spectrometry, a revolution in clinical microbial identification. Clin. Microbiol Infect. 2010, 16, 1614–1619. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  46. Wang, H.Y.; Kim, S.; Kim, J.; Park, S.D.; Uh, Y.; Lee, H. Multiplex real-time PCR assay for rapid detection of methicillin-resistant staphylococci directly from positive blood cultures. J. Clin. Microbiol. 2014, 52, 1911–1920. [Google Scholar] [CrossRef] [Green Version]
  47. Monecke, S.; Ehricht, R. Rapid genotyping of methicillin-resistant Staphylococcus aureus (MRSA) isolates using miniaturised oligonucleotide arrays. Clin. Microbiol Infect. 2005, 11, 825–833. [Google Scholar] [CrossRef] [Green Version]
  48. Strauß, L.; Ruffing, U.; Abdulla, S.; Alabi, A.; Akulenko, R.; Garrine, M.; Germann, A.; Grobusch, M.P.; Helms, V.; Herrmann, M.; et al. Detecting Staphylococcus aureus virulence and resistance genes: A comparison of whole-genome sequencing and DNA microarray technology. J. Clin. Microbiol. 2016, 54, 1008–1016. [Google Scholar] [CrossRef] [Green Version]
  49. Monecke, S.; Slickers, P.; Ehricht, R. Assignment of Staphylococcus aureus isolates to clonal complexes based on microarray analysis and pattern recognition. FEMS Immunol Med. Microbiol. 2008, 53, 237–251. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  50. Krzywinski, M.; Schein, J.; Birol, I.; Connors, J.; Gascoyne, R.; Horsman, D.; Jones, S.J.; Marra, M.A. Circos: An information aesthetic for comparative genomics. Genome Res. 2009, 19, 1639–1645. [Google Scholar] [CrossRef] [Green Version]
  51. Lozano, C.; López, M.; Gómez-Sanz, E.; Ruiz-Larrea, F.; Torres, C.; Zarazaga, M. Detection of methicillin-resistant Staphylococcus aureus ST398 in food samples of animal origin in Spain. J. Antimicrob Chemother. 2009, 64, 1325–1326. [Google Scholar] [CrossRef] [Green Version]
  52. Mairi, A.; Touati, A.; Pantel, A.; Zenati, K.; Martinez, A.Y.; Dunyach-Remy, C.; Sotto, A.; Lavigne, J.P. Distribution of toxinogenic methicillin-resistant and methicillin-susceptible Staphylococcus aureus from different ecological niches in Algeria. Toxins. 2019, 11, 500. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  53. Pu, S.; Han, F.; Ge, B. Isolation and characterization of methicillin-resistant Staphylococcus aureus strains from Louisiana retail meats. Appl Environ. Microbiol. 2009, 75, 265–267. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  54. Olaniyi, R.; Pozzi, C.; Grimaldi, L.; Bagnoli, F. Staphylococcus aureus-associated skin and soft tissue infections: Anatomical localization, epidemiology, therapy and potential prophylaxis. Curr Top. Microbiol Immunol. 2017, 409, 199–227. [Google Scholar] [PubMed]
  55. Akkou, M.; Bouchiat, C.; Antri, K.; Bes, M.; Tristan, A.; Dauwalder, O.; Martins-Simoes, P.; Rasigade, J.P.; Etienne, J.; Vandenesch, F.; et al. New host shift from human to cows within Staphylococcus aureus involved in bovine mastitis and nasal carriage of animal’s caretakers. Vet. Microbiol. 2018, 223, 173–180. [Google Scholar] [CrossRef]
  56. Hata, E.; Katsuda, K.; Kobayashi, H.; Uchida, I.; Tanaka, K.; Eguchi, M. Genetic variation among Staphylococcus aureus strains from bovine milk and their relevance to methicillin-resistant isolates from humans. Journal of clinical microbiology 2010, 48, 2130–2139. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  57. Pantosti, A. Methicillin-Resistant Staphylococcus aureus Associated with Animals and Its Relevance to Human Health. Frontiers in microbiology 2012, 3, 127. [Google Scholar] [CrossRef] [Green Version]
  58. Luedicke, C.; Slickers, P.; Ehricht, R.; Monecke, S. Molecular fingerprinting of Staphylococcus aureus from bone and joint infections. Eur J. Clin. Microbiol Infect. Dis. 2010, 29, 457–463. [Google Scholar] [CrossRef]
  59. Monecke, S.; Coombs, G.; Shore, A.C.; Coleman, D.C.; Akpaka, P.; Borg, M.; Chow, H.; Ip, M.; Jatzwauk, L.; Jonas, D.; et al. A field guide to pandemic, epidemic and sporadic clones of methicillin-resistant Staphylococcus aureus. PLoS ONE 2011, 6, 0017936. [Google Scholar] [CrossRef] [PubMed]
  60. Schmidt, T.; Kock, M.M.; Ehlers, M.M. Molecular characterization of Staphylococcus aureus isolated from bovine mastitis and close human contacts in South African dairy herds: Genetic diversity and inter-species host transmission. Front. Microbiol. 2017, 8, 511. [Google Scholar] [CrossRef] [Green Version]
  61. Wu, S.; Huang, J.; Wu, Q.; Zhang, J.; Zhang, F.; Yang, X.; Wu, H.; Zeng, H.; Chen, M.; Ding, Y.; et al. Staphylococcus aureus Isolated From Retail Meat and Meat Products in China: Incidence, Antibiotic Resistance and Genetic Diversity. Front. Microbiol. 2018, 9, 2767. [Google Scholar] [CrossRef]
  62. Bar-Gal, G.K.; Blum, S.E.; Hadas, L.; Ehricht, R.; Monecke, S.; Leitner, G. Host-specificity of Staphylococcus aureus causing intramammary infections in dairy animals assessed by genotyping and virulence genes. Vet. Microbiol. 2015, 176, 143–154. [Google Scholar] [CrossRef] [PubMed]
  63. Jamil, B.; Gawlik, D.; Syed, M.A.; Shah, A.A.; Abbasi, S.A.; Müller, E.; Reißig, A.; Ehricht, R.; Monecke, S. Hospital-acquired methicillin-resistant Staphylococcus aureus (MRSA) from Pakistan: Molecular characterisation by microarray technology. European Journal of Clinical Microbiology & Infectious Diseases 2018, 37, 691–700. [Google Scholar] [CrossRef]
  64. Fessler, A.T.; Kadlec, K.; Hassel, M.; Hauschild, T.; Eidam, C.; Ehricht, R.; Monecke, S.; Schwarz, S. Characterization of methicillin-resistant Staphylococcus aureus isolates from food and food products of poultry origin in Germany. Appl Environ. Microbiol. 2011, 77, 7151–7157. [Google Scholar] [CrossRef] [Green Version]
  65. Ogata, K.; Narimatsu, H.; Suzuki, M.; Higuchi, W.; Yamamoto, T.; Taniguchi, H. Commercially distributed meat as a potential vehicle for community-acquired methicillin-resistant Staphylococcus aureus. Appl Environ. Microbiol. 2012, 78, 2797–2802. [Google Scholar] [CrossRef] [Green Version]
  66. Petinaki, E.; Spiliopoulou, I. Methicillin-resistant Staphylococcus aureus among companion and food-chain animals: Impact of human contacts. Clin. Microbiol Infect. 2012, 18, 626–634. [Google Scholar] [CrossRef] [Green Version]
  67. Bekkhoucha, S.N.; Cady, A.; Gautier, P.; Itim, F.; Donnio, P.Y. A portrait of Staphylococcus aureus from the other side of the Mediterranean Sea: Molecular characteristics of isolates from Western Algeria. Eur J. Clin. Microbiol Infect. Dis 2009, 28, 553–555. [Google Scholar] [CrossRef] [PubMed]
  68. Ben Nejma, M.; Mastouri, M.; Bel Hadj Jrad, B.; Nour, M. Characterization of ST80 Panton-Valentine leukocidin-positive community-acquired methicillin-resistant Staphylococcus aureus clone in Tunisia. Diagn Microbiol Infect. Dis. 2013, 77, 20–24. [Google Scholar] [CrossRef]
  69. Udo, E.E.; O’Brien, F.G.; Al-Sweih, N.; Noronha, B.; Matthew, B.; Grubb, W.B. Genetic lineages of community-associated methicillin-resistant Staphylococcus aureus in Kuwait hospitals. J. Clin. Microbiol 2008, 46, 3514–3516. [Google Scholar] [CrossRef] [Green Version]
  70. Knight, G.M.; Budd, E.L.; Whitney, L.; Thornley, A.; Al-Ghusein, H.; Planche, T.; Lindsay, J.A. Shift in dominant hospital-associated methicillin-resistant Staphylococcus aureus (HA-MRSA) clones over time. J. Antimicrob Chemother. 2012, 67, 2514–2522. [Google Scholar] [CrossRef] [Green Version]
  71. Price, L.B.; Stegger, M.; Hasman, H.; Aziz, M.; Larsen, J.; Andersen, P.S.; Pearson, T.; Waters, A.E.; Foster, J.T.; Schupp, J.; et al. Staphylococcus aureus CC398: Host adaptation and emergence of methicillin resistance in livestock. mBio. 2012, 3, 00305–00311. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  72. Witte, W.; Strommenger, B.; Stanek, C.; Cuny, C. Methicillin-resistant Staphylococcus aureus ST398 in humans and animals, Central Europe. Emerg Infect. Dis 2007, 13, 255–258. [Google Scholar] [CrossRef]
  73. Cuny, C.; Wieler, L.H.; Witte, W. Livestock-associated MRSA: The impact on humans. Antibiotics. 2015, 4, 521–543. [Google Scholar] [CrossRef] [PubMed]
  74. Knox, J.; Uhlemann, A.; Lowy, F.D. Staphylococcus aureus infections: Transmission within households and the community. Trends Microbiol. 2015, 23, 437–444. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  75. Herron-Olson, L.; Fitzgerald, J.R.; Musser, J.M.; Kapur, V. Molecular correlates of host specialization in Staphylococcus aureus. PLoS ONE. 2007, 2, e1120. [Google Scholar] [CrossRef]
  76. Monecke, S.; Luedicke, C.; Slickers, P.; Ehricht, R. Molecular epidemiology of Staphylococcus aureus in asymptomatic carriers. Eur J. Clin. Microbiol Infect. Dis. 2009, 28, 1159–1165. [Google Scholar] [CrossRef] [PubMed]
  77. Melles, D.C.; Tenover, F.C.; Kuehnert, M.J.; Witsenboer, H.; Peeters, J.K.; Verbrugh, H.A.; van Belkum, A. Overlapping population structures of nasal isolates of Staphylococcus aureus from healthy Dutch and American individuals. J. Clin. Microbiol. 2008, 46, 235–241. [Google Scholar] [CrossRef] [Green Version]
  78. Basanisi, M.G.; La Bella, G.; Nobili, G.; Franconieri, I.; La Salandra, G. Genotyping of methicillin-resistant Staphylococcus aureus (MRSA) isolated from milk and dairy products in South Italy. Food Microbiol. 2017, 62, 141–146. [Google Scholar] [CrossRef] [Green Version]
  79. Woolhouse, M.; Ward, M.; van Bunnik, B.; Farrar, J. Antimicrobial resistance in humans, livestock and the wider environment. Philos Trans. R Soc. Lond B Biol Sci 2015, 370. [Google Scholar] [CrossRef]
  80. Schlotter, K.; Ehricht, R.; Hotzel, H.; Monecke, S.; Pfeffer, M.; Donat, K. Leukocidin genes lukF-P83 and lukM are associated with Staphylococcus aureus clonal complexes 151, 479 and 133 isolated from bovine udder infections in Thuringia, Germany. Vet. Res. 2012, 43, 42. [Google Scholar] [CrossRef] [Green Version]
  81. Boss, R.; Cosandey, A.; Luini, M.; Artursson, K.; Bardiau, M.; Breitenwieser, F.; Hehenberger, E.; Lam, T.; Mansfeld, M.; Michel, A.; et al. Bovine Staphylococcus aureus: Subtyping, evolution, and zoonotic transfer. J. Dairy Sci. 2016, 99, 515–528. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  82. Käppeli, N.; Morach, M.; Corti, S.; Eicher, C.; Stephan, R.; Johler, S. Staphylococcus aureus related to bovine mastitis in Switzerland: Clonal diversity, virulence gene profiles, and antimicrobial resistance of isolates collected throughout 2017. J. Dairy Sci. 2019, 102, 3274–3281. [Google Scholar] [CrossRef] [Green Version]
  83. Jørgensen, H.J.; Mathisen, T.; Løvseth, A.; Omoe, K.; Qvale, K.S.; Loncarevic, S. An outbreak of staphylococcal food poisoning caused by enterotoxin H in mashed potato made with raw milk. FEMS Microbiol Lett. 2005, 252, 267–272. [Google Scholar] [CrossRef] [Green Version]
  84. Dinges, M.M.; Orwin, P.M.; Schlievert, P.M. Exotoxins of Staphylococcus aureus. Clin. Microbiol Rev. 2000, 13, 16–34. [Google Scholar] [CrossRef]
  85. Arciola, C.R.; Campoccia, D.; Ravaioli, S.; Montanaro, L. Polysaccharide intercellular adhesin in biofilm: Structural and regulatory aspects. Front. Cell Infect. Microbiol. 2015, 5. [Google Scholar] [CrossRef] [Green Version]
  86. Mirani, Z.A.; Aziz, M.; Khan, M.N.; Lal, I.; Hassan, N.U.; Khan, S.I. Biofilm formation and dispersal of Staphylococcus aureus under the influence of oxacillin. Microb Pathog. 2013, 62, 66–72. [Google Scholar] [CrossRef] [PubMed]
  87. Kim, Y.J.; Oh, D.H.; Song, B.R.; Heo, E.J.; Lim, J.S.; Moon, J.S.; Park, H.J.; Wee, S.H.; Sung, K. Molecular characterization, antibiotic resistance, and virulence factors of methicillin-resistant Staphylococcus aureus strains isolated from imported and domestic meat in Korea. Foodborne Pathog Dis. 2015, 12, 390–398. [Google Scholar] [CrossRef] [PubMed]
  88. Parisi, A.; Caruso, M.; Normanno, G.; Latorre, L.; Sottili, R.; Miccolupo, A.; Fraccalvieri, R.; Santagada, G. Prevalence, antimicrobial susceptibility and molecular typing of methicillin-resistant Staphylococcus aureus (MRSA) in bulk tank milk from southern Italy. Food Microbiol. 2016, 58, 36–42. [Google Scholar] [CrossRef]
  89. Kesah, C.; Ben Redjeb, S.; Odugbemi, T.O.; Boye, C.S.; Dosso, M.; Ndinya Achola, J.O.; Koulla-Shiro, S.; Benbachir, M.; Rahal, K.; Borg, M. Prevalence of methicillin-resistant Staphylococcus aureus in eight African hospitals and Malta. Clin. Microbiol Infect. 2003, 9, 153–156. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  90. Alioua, M.A.; Labid, A.; Amoura, K.; Bertine, M.; Gacemi-Kirane, D.; Dekhil, M. Emergence of the European ST80 clone of community-associated methicillin-resistant Staphylococcus aureus as a cause of healthcare-associated infections in Eastern Algeria. Med. Mal. Infect. 2014, 44, 180–183. [Google Scholar] [CrossRef]
  91. Ouchenane, Z.; Smati, F.; Rolain, J.M.; Raoult, D. Molecular characterization of methicillin-resistant Staphylococcus aureus isolates in Algeria. Pathologie Biologie 2011, 59, e129–e132. [Google Scholar] [CrossRef]
  92. Rebiahi, S.A.; Abdelouahid, D.E.; Rahmoun, M.; Abdelali, S.; Azzaoui, H. Emergence of vancomycin-resistant Staphylococcus aureus identified in the Tlemcen university hospital (North-West Algeria). Med. Mal. Infect. 2011, 41, 646–651. [Google Scholar] [CrossRef]
  93. Barour, D.; Berghiche, A.; Boulebda, N. Antimicrobial resistance of Escherichia coli isolates from cattle in Eastern Algeria. Vet. World. 2019, 12, 1195–1203. [Google Scholar] [CrossRef] [PubMed]
  94. Benrabia, I.; Hamdi, T.M.; Shehata, A.A.; Neubauer, H.; Wareth, G. Methicillin-resistant Staphylococcus aureus (MRSA) in poultry species in Algeria: Long-term study on prevalence and antimicrobial resistance. Vet. Sci. 2020, 7, 54. [Google Scholar] [CrossRef] [PubMed]
  95. Dermota, U.; Jurca, T.; Harlander, T.; Košir, M.; Zajc, U.; Golob, M.; Zdovc, I.; Košnik, I.G. Infections caused by community-associated methicillin-resistant Staphylococcus aureus European clone (ST80) in Slovenia between 2006 And 2013. Zdr Varst. 2016, 55, 121–125. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  96. Larsen, A.R.; Böcher, S.; Stegger, M.; Goering, R.; Pallesen, L.V.; Skov, R. Epidemiology of european community-associated methicillin-resistant Staphylococcus aureus clonal complex 80 type IV strains isolated in Denmark from 1993 to 2004. J. Clin. Microbiol. 2008, 46, 62. [Google Scholar] [CrossRef] [PubMed] [Green Version]
Pathogens 10 01276 g001 550
Figure 1. Graphic visualization of source of the isolates (clinical, food and nasal swabs) in circular layout [50], revealing the association between the MSCRAMMs genes, methicillin resistance and SCCmec Typing, capsule/biofilm-associated genes, virulence-associated genes, toxin genes, antibiotic resistance genes, accessory gene regulator allele, and the clonal complexes detected by microarray using interconnections with a variety of colored ribbons. The circumference (track) of the circle is divided into arcs of varying lengths according to the abundance of every single factor.
Figure 1. Graphic visualization of source of the isolates (clinical, food and nasal swabs) in circular layout [50], revealing the association between the MSCRAMMs genes, methicillin resistance and SCCmec Typing, capsule/biofilm-associated genes, virulence-associated genes, toxin genes, antibiotic resistance genes, accessory gene regulator allele, and the clonal complexes detected by microarray using interconnections with a variety of colored ribbons. The circumference (track) of the circle is divided into arcs of varying lengths according to the abundance of every single factor.
Pathogens 10 01276 g001
Table
Table 1. Assignment of 60 S. aureus isolated from different samples and their origin.
Table 1. Assignment of 60 S. aureus isolated from different samples and their origin.
Clonal ComplexSource of IsolatesTotal CC
Clinical SamplesFood SamplesNasal Swabs
SourceIsolates NumberTotalSourceIsolates NumberTotalIsolates NumberTotal
CC1-MSSABlood culture13Raw milk410--13
Pus1Chicken meat1
Surgical wound1Minced beef meat4
Sausages1
CC5-MSSAUrine12Minced beef meat22--4
Vaginal discharge1
CC6-MRSA IVCatheter23Minced beef meat22--5
Pus1
CC80-MRSA IVSperm16Minced beef meat11118
Pus4
Urine1
CC97-MSSAThroat fluid11Creamy cake281110
Raw milk5
Minced beef meat1
CC15-MSSAPus22---224
CC22-MRSA-IVPus11---334
CC30-MSSAPus11---112
CC8-MSSAUrine11-----1
CC479-MSSA---Raw milk11--1
CC22-MSSA------444
CC398-MSSA------111
CC45-MSSA------222
CC705-MSSA------111
Total 20 24 1660
Table
Table 2. Distribution of virulence-associated genes in S. aureus isolates.
Table 2. Distribution of virulence-associated genes in S. aureus isolates.
Clonal Complex
(n)		Origin *
(n)		agr Group
(n)		Virulence-Associated GenesCapsule/Biofilm-Associated GenesToxin Genes
lukFS-PVlukF-PV (P83)luk-MlukF-hlglukS-hlghlgAhlahlbedinBcap5cap8icaACDseasebsecsehsekegctst1etD
CC1-MSSA (13)C (3)agr III (3)---33333--3331-33---
F (10)agr III (10)---1010101010--10103--103---
CC5-MSSA (4)C (2)agr III (2)---22222-2-22----2--
F (2)agr III (2)---22222-2-22----2--
CC6-MRSA IVC (3)agr I (3)---33333--333-------
F (2)agr I (2)---22222--222-------
CC8-MSSA (1)C (1)agr I (1)---11111-1-11-1-----
CC15-MSSA (4)C (2)agr II (2)---2222---22--------
N (2)agr II (2)---2222---22--------
CC22-MSSA (4)N (4)agr I (4)---44444-4-4-----44 §-
CC22-MRSA- IV (4)C (1)agr I (1)---11111-1-1-----11 §-
N (3)agr I (3)---32323-3-3-----33 §-
CC30-MSSA(2)C (1)agr III (1)- -1111---11-----1--
N(1)agr III (1)---11111--111----1--
CC45-MSSA (2)N(2)agr I (2)---2222---22--1--2--
CC80-MRSA- IV (8)C (6)agr III (6)6--666666-66-------6
N (1)agr III (1)1--111111-11-------1
F (1)agr III (1)1--111111-11-------1
CC97-MSSA (10)C (1)agr I (1)---11111-1-1-1------
N (1)agr I (1)---11111-1-1-1------
F (8)agr I (8)---88888-8-8-2------
CC398-MSSA (1)N (1)agr I (1)---11111-1-1--------
CC479- MSSAF (1)agr II (1)-1111111--11-----1-1
CC705-MSSAN (1)agr II (1)-1111111--11-----1--
* C: clinical isolates; F: food isolates; N: isolates from nasal swabs. § toxic shock syndrome toxin-1 tst1 (“human” allele).
Table
Table 3. Distribution of MSCRAMM genes in S. aureus isolates.
Table 3. Distribution of MSCRAMM genes in S. aureus isolates.
Clonal Complex
(n)		Origin *
(n)		agr Group
(n)		MSCRAMM Genes
bbpclfA/BcnaebhepbsEnofibfnbAfnbBmapsasGsdrCsdrDvwb
CC1-MSSA (13)C (3)agr III (3)33333333333333
F (10)agr III (10)101010101010101091010101010
CC5-MSSA (4)C (2)agr III (2)22-22222222222
F (2)agr III (2)22-22222222222
CC6-MRSA IV (5)C (3)agr I (3)33333333333333
F (2)agr I (2)22222222222222
CC8-MSSA (1)C (1)agr I (1)11-11111111111
CC15-MSSA (4)C (2)agr II (2)22-22222222222
N (2)agr II (2)22-22222222222
CC22-MSSA (4)N (4)agr I (4)444444-4-44444
CC22-MRSA- IV (4)C (1)agr I (1)111-11-1-11111
N (3)agr I (3)333-33-3-33333
CC30-MSSA (2)C (1)agr III (1)111111-1-1-111
N(1)agr III (1)111111-1-1-111
CC45-MSSA (2)N(2)agr I (2)222222-222-2-2
CC80-MRSA- IV (8)C (6)agr III (6)66-66666666666
N (1)agr III (1)11-11111111111
F (1)agr III (1)11-11111111111
CC97-MSSA (10)C (1)agr I (1)11-11111111111
N (1)agr I (1)11-11111111111
F (8)agr I (8)68-88888788888
CC398-MSSA (1)N (1)agr I (1)-11111-111-111
CC479- MSSA (1)F (1)agr II (1)-11111111111-1
CC705-MSSA (1)N (1)agr II (1)11-11111-1-1-1
* C: clinical isolates; F: food isolates; N: isolates from nasal swabs.
Table
Table 4. Antimicrobial resistance-associated genes detected in 60 S. aureus isolates.
Table 4. Antimicrobial resistance-associated genes detected in 60 S. aureus isolates.
Clonal Complex
(n) *		Origin
(n) *		Antimicrobial Resistance Genes (n)
mecASCCmecblaZermBermCaphA3aadDsatfusCfar1tetMtetKfosB
CC1-MSSA (13)F (10)-ccrAB1 (10)3--1-110----
C (3)-ccrAB1 (3)2-----3-11-
CC5-MSSA (4)C (2)------------2
F (2)------------2
CC6-MRSA IV (5)C (3)3ccrAB2 (3)3-3-------3
F (2)2ccrAB2 (2)1-2-------2
CC8-MSSA (1)C (1)--1-------1-1
CC15-MSSA (4)C (2)--2---1----22
N (2)--2---------2
CC22-MSSA (4)N (4)--4----------
CC22-MRSA- IV (4)C (1)1ccrAB2 (1)1----------
N (3)4ccrAB2 (3)3----------
CC30-MSSA (2)C (1)--1---------1
N (1)--1---------1
CC45-MSSA (2)N (2)--2----------
CC80-MRSA- IV (8)C (6)6ccrAB2 (6)6-16-6-6-6-
N (1)1ccrAB2 (1)---1-1-----
F (1)1ccrAB2 (1)1-11-1-1-1-
CC97-MSSA (10)C (1)--1--1 1-----
N (1)--1--1 1-----
F (8)--82-2 2--14-
CC398-MSSA (1)N (1)-------------
CC479-MSSA (1)F (1)-----------1-
CC705-MSSA (1)N (1)-------------
* N: number of isolates; C: Clinical samples; F: Food samples; N: Nasal samples.
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Achek, R.; El-Adawy, H.; Hotzel, H.; Hendam, A.; Tomaso, H.; Ehricht, R.; Neubauer, H.; Nabi, I.; Hamdi, T.M.; Monecke, S. Molecular Characterization of Staphylococcus aureus Isolated from Human and Food Samples in Northern Algeria. Pathogens 2021, 10, 1276. https://doi.org/10.3390/pathogens10101276

AMA Style

Achek R, El-Adawy H, Hotzel H, Hendam A, Tomaso H, Ehricht R, Neubauer H, Nabi I, Hamdi TM, Monecke S. Molecular Characterization of Staphylococcus aureus Isolated from Human and Food Samples in Northern Algeria. Pathogens. 2021; 10(10):1276. https://doi.org/10.3390/pathogens10101276

Chicago/Turabian Style

Achek, Rachid, Hosny El-Adawy, Helmut Hotzel, Ashraf Hendam, Herbert Tomaso, Ralf Ehricht, Heinrich Neubauer, Ibrahim Nabi, Taha Mossadak Hamdi, and Stefan Monecke. 2021. "Molecular Characterization of Staphylococcus aureus Isolated from Human and Food Samples in Northern Algeria" Pathogens 10, no. 10: 1276. https://doi.org/10.3390/pathogens10101276

APA Style

Achek, R., El-Adawy, H., Hotzel, H., Hendam, A., Tomaso, H., Ehricht, R., Neubauer, H., Nabi, I., Hamdi, T. M., & Monecke, S. (2021). Molecular Characterization of Staphylococcus aureus Isolated from Human and Food Samples in Northern Algeria. Pathogens, 10(10), 1276. https://doi.org/10.3390/pathogens10101276

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop