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Article

High Prevalence of ESBL and Plasmid-Mediated Quinolone Resistance Genes in Salmonella enterica Isolated from Retail Meats and Slaughterhouses in Egypt

by
Wesam A. Adel
1,
Ashraf M. Ahmed
1,*,
Yamen Hegazy
2,
Helmy A. Torky
3 and
Tadashi Shimamoto
4,*
1
Department of Bacteriology, Mycology and Immunology, Faculty of Veterinary Medicine, Kafrelsheikh University, Kafr El-Sheikh 33516, Egypt
2
Department of Animal Medicine, Faculty of Veterinary Medicine, Kafrelsheikh University, Kafr El-Sheikh 33516, Egypt
3
Department of Microbiology, Faculty of Veterinary Medicine, Alexandria University, Alexandria 22758, Egypt
4
Laboratory of Food Microbiology and Hygiene, Graduate School of Integrated Sciences for Life, Hiroshima University, Higashihiroshima 739-8528, Japan
*
Authors to whom correspondence should be addressed.
Antibiotics 2021, 10(7), 881; https://doi.org/10.3390/antibiotics10070881
Submission received: 22 June 2021 / Revised: 16 July 2021 / Accepted: 18 July 2021 / Published: 20 July 2021
(This article belongs to the Section Mechanism and Evolution of Antibiotic Resistance)
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Abstract

:
The emergence and spread of multidrug-resistant Salmonella enterica (S. enterica) to humans through food of animal origin are considered a major global public health concern. Currently, little is known about the prevalence of important antimicrobial resistance genes in S. enterica from retail food in Africa. Therefore, the screening and characterization of the extended-spectrum β-lactamase (ESBL) and plasmid-mediated quinolone resistance (PMQR) genes in S. enterica isolated from retail meats and slaughterhouses in Egypt were done by using PCR and DNA sequencing techniques. Twenty-eight out of thirty-four (82.4%) non-duplicate S. enterica isolates showed multidrug-resistance phenotypes to at least three classes of antimicrobials, and fourteen (41.2%) exhibited an ESBL-resistance phenotype and harbored at least one ESBL-encoding gene. The identified β-lactamase-encoding genes included blaCTX-M-1, blaCTX-M-3, blaCTX-M-13, blaCTX-M-14, blaCTX-M-15, and blaSHV-12 (ESBL types); blaCMY-2 (AmpC type); and blaTEM-1 and blaOXA-1 (narrow-spectrum types). PMQR genes (included qnrA, qnrB, qnrS, and aac(6′)-Ib-cr) were identified in 23 (67.6%) isolates. The presence of ESBL- and PMQR-producing S. enterica with a high prevalence rate in retail meats and slaughterhouses is considered a major threat to public health as these strains with resistance genes could be transmitted to humans through the food chain.

1. Introduction

Food safety is a significant global public health concern. Unsafe food can lead to the transmission of a wide range of foodborne illnesses and outbreaks. According to a recent report from the WHO, an estimated 600 million (approximately 1 in 10 people worldwide) get ill after eating contaminated food and 420,000 die every year, resulting in the loss of 33 million disability-adjusted life years [1]. Currently, the recommended treatment options for salmonellosis include extended-spectrum cephalosporins and fluoroquinolones, as resistance to older antimicrobials (e.g., ampicillin, trimethoprim-sulfamethoxazole, and chloramphenicol) has been increasing for several years [2]. In recent years, the emergence of non-typhoidal Salmonella enterica with multidrug resistance to the extended-spectrum cephalosporins and fluoroquinolones has posed a serious global public health concern [3]. The resistance to cephalosporins and fluoroquinolones, as critically important antibiotics for human health, will lead to increased severity, morbidity, and mortality of salmonellosis in humans and consequently the use of last-line antimicrobials (e.g., carbapenems) [4]. In developing countries, this problem is intensified by the misuse and overuse of antimicrobial agents in humans, animals, poultry, and aquatic systems [5]. In many African countries, street food vending has become increasingly important to poorer economies; however, such foods are prepared under poor sanitation and unhygienic environments [6]. The majority of developed countries utilize a regular surveillance and monitoring system for antimicrobial drug resistance (AMR) that is updated regularly [7]. For example, the National Antimicrobial Resistance Monitoring Systems (NARMS) in the United States and the Danish Integrated Antimicrobial Resistance Monitoring and Research Programme (DANMAP) in Denmark [8,9]. Therefore, the AMR phenomenon is well mapped and monitored in these countries [10]. Alternatively, in developing countries, there is no regular surveillance or monitoring system for AMR, owing to the lack of surveillance networks, laboratory capacity, and appropriate diagnostics [11]. Recently, many studies have been conducted in both developed and developing countries to monitor the prevalence of ESBL-producing S. enterica in meat products, such as the United States [12], Italy [13], Chile [14], Bangladesh [15], and Brazil [16]. Currently, there is a considerable lack of information related to tracking and monitoring the emergence and incidence of antimicrobial resistance genes in pathogenic bacteria from food in Africa. Notably, between January and September 2010, we carried out the first large-scale survey in Africa to estimate the prevalence of antimicrobial resistance genes in S. enterica isolated from retail meat and dairy products in Egypt [17]. Therefore, the objectives of this study were to monitor the prevalence of extended-spectrum β-lactamase (ESBL) and plasmid-mediated quinolone resistance (PMQR) genes in S. enterica isolated from retail meats and slaughterhouses in Egypt and also to compare the change in the prevalence rates of ESBL and PMQR genes with those previously reported by our team ten years ago [17].

2. Results

2.1. Prevalence of MDR and ESBL-Producing S. enterica Isolated from Retail Meat and Beef Carcasses

In this study, non-duplicate isolates of S. enterica were detected in 34 (11.3%) of the 400 samples (chicken and beef meat and beef carcass swabs) analyzed. S. enterica isolates were serologically categorized into ten S. enterica serovars. (Figure 1, Supplementary Table S1). Twenty-eight out of 34 (82.4%) S. enterica isolates showed MDR phenotypes to at least three classes of antimicrobials. MDR was defined as isolates showing resistance to three or more antimicrobial classes [18]. The most prevalent resistance was to ampicillin, streptomycin, oxacillin, and tetracycline. Additionally, 14 (41.2%) of 34 S. enterica isolates showed ESBL-resistant phenotypes (Figure 2, Table 1, Supplementary Tables S2 and S3).

2.2. Prevalence of β-Lactamase-Encoding Genes in S. enterica Isolated from Retail Meat and Beef Carcasses in Egypt

PCR and DNA sequencing identified the CTX-M-encoding gene blaCTX-M in 11 (32.4%) S. enterica isolates. The SHV-encoding gene blaSHV-12 was identified in 5 (14.7%) S. enterica isolates (Table 2). Additionally, the AmpC β-lactamase-encoding gene blaCMY-2 was identified in 9 isolates (26.5%) of S. enterica (Table 2). Finally, the narrow-spectrum β-lactamase-encoding genes blaTEM-1 and blaOXA-1 were identified in 27 (79.4%) and 10 (29.4%) S. enterica isolates, respectively (Table 2). Of note, the resistance phenotypes were expressed for all β-lactamase-encoding genes (Table 1).

2.3. Prevalence of Plasmid-Mediated Quinolone Resistance Genes in S. enterica Isolated from Retail Meats and Beef Carcasses in Egypt

Multiplex PCR screening identified plasmid-mediated quinolone resistance (PMQR) genes in 23 (67.6%) S. enterica isolates. The prevalence of PMQR genes was as follows: qnrS in 12 (35.3%) S. enterica isolates, qnrB in 8 (23.5%) S. enterica isolates, and aac(6′)-Ib-cr in 7 (23.5%) isolates (Table 1 and Table 2). Of note, all qnr containing isolates were resistant to nalidixic acid, and some of them were resistant to both nalidixic acid and ciprofloxacin (Table 1).

2.4. Comparison between the Prevalence Rates of Resistance Phenotypes and Genes in Salmonella Enterica Isolated from Retail Meats and Beef Carcasses in 2010 and 2020 in Egypt

Regarding a comparison between our results in the previous study in 2010 and the current study: MDR S. enterica was detected with prevalence rates: 69.8% and 82.4%, respectively; ESBL-resistant S. enterica with prevalence rates: 17% and 41.2%, respectively; β-lactamase-encoding genes with prevalence rates: 75.1% and 91.2%, respectively; and finally, PMQR genes with prevalence rates: 28.3% and 67.6%, respectively (Figure 3, Supplementary Table S4).

2.5. Transferability and Replicon Typing of Plasmids

PCR screening for replicon typing of plasmids revealed the presence of the following incompatibility groups: IncI1 in 9 (26.5%); IncA/C in 8 (23.5%); IncN in 7 (20.6%); IncHI1 in 5 (14.7%); IncHI1 in 4 (11.8%); and IncL/M in 1 (2.9%) S. enterica isolate (Supplementary Table S5). Moreover, the results of conjugation experiments showed that plasmids are conjugable in 26 (76.5%) S. enterica isolates, with most resistance genes transferred to the transconjugant E. coli HB101 (Supplementary Table S5).

3. Discussion

3.1. High Prevalence of MDR and ESBL-Producing S. enterica Isolated from Retail Meat and Beef Carcasses in Egypt

Antimicrobial resistance (AMR) is an increasingly growing problem that represents a threat to our capacity to treat common bacterial infections. AMR has recently been considered one of the top 10 global public health threats facing humanity according to WHO’s report [19]. The rapid and high global spread of multidrug-resistant bacteria that cause infections that cannot be treated with existing antimicrobial agents is particularly alarming [19]. The emergence and spread of multidrug-resistant (MDR) bacteria have led to the exacerbation of the AMR phenomenon worldwide due to the misuse and overuse of antimicrobials [1]. In the United States, at least 2 million people per annum acquire serious bacterial infections that are resistant to one or more of the antibiotics designed to treat those infections. Additionally, at least 23,000 people die annually as a direct result of these antibiotic-resistant infections [20]. Multidrug-resistant S. enterica spreads from animals to people predominantly through food [21]. In the USA, the CDC notes resistance to ceftriaxone and some level of resistance to ciprofloxacin in approximately 3% of non-typhoidal S. enterica tested. Approximately 5% of non-typhoidal S. enterica tested by the CDC are resistant to five or more types of drugs [20].
The prevalence of MDR S. enterica in meat products varies among different countries. In our study, MDR S. enterica was detected in 82.4% of retail meat samples. This prevalence rate is considerably higher compared to our previous report (69.8%) on MDR S. enterica in retail meats collected in 2010 in Egypt [17] (Figure 3, Supplementary Table S4) and also compared to that recently reported (68.5%) in China for MDR S. Enteritidis strains collected from retail foods in 39 cities [22] and that reported (50.9%) in South Korea for MDR S. enterica isolated from retail chicken meat [23]. However, it is relatively low compared to another recent study from Egypt, which showed all (100%) S. enterica serovars isolated from retail chickens were MDR [24]. Additionally, the prevalence of ESBL-resistant S. enterica isolates increased significantly from 17% in 2010 to 41.2% in the current study (Figure 3, Supplementary Table S3). Alternatively, our results are considered relatively low compared to that recently reported in chicken meat from Bangladesh as all (100%) S. enterica isolates were MDR and 58.1% of isolates were ESBL producers [15]. Additionally, a recent report from Italy showed that 80.5% of S. Infantis isolates from a broiler food chain exhibited ESBL phenotypes [13]. Similarly, 94% of S. Infantis isolates from chicken meat in Chile were MDR, and 63.2% were broad-spectrum β-lactam resistant [14]. Notably, raw chicken and sushi in Spain are the riskiest products in terms of transmission of ESBL-producing Enterobacteriaceae (occurrence 53.1% and 19.4%, respectively) [25]. Of note, our results are also considered relatively low compared to that we have recently reported from retail fishes in Egypt, as all (100%) S. enterica isolates were MDR and 57.9% of isolates were ESBL producers [26].

3.2. High Prevalence of β-Lactamase-Encoding Genes in S. enterica Isolated from Retail Meat and Beef Carcasses in Egypt

The production of β-lactamases is considered the main mechanism of resistance to β-lactam antibiotics in bacteria. The most common types of β-lactamases are categorized as follows: narrow-spectrum β-lactamases (TEM-1 and OXA-1) primarily confer resistance to first- and second-generation cephalosporins; AmpC β-lactamase (CMY) confers resistance to cephamycins (such as cefoxitin and cefotetan), and ESBLs (mainly CTX-M and SHV) confer resistance to expanded-spectrum cephalosporins, such as third- and fourth-generation cephalosporins [27,28]. The resistance of S. enterica to extended-spectrum cephalosporins is of major concern as these antibiotics are usually used as a front-line treatment for typhoid fever and other S. enterica infections in hospitals [29]. In this study, PCR and DNA sequencing showed that ESBL-producing S. enterica isolates carried at least one ESBL-encoding gene. These genes included blaCTX-M (types 1, 2, 3, 13, 14, and 15) in S. enterica isolates (S. Typhimurium, S. Enteriditis, S. Infantis, S. Kentucky, and S. Virchow) and blaSHV-12 in S. enterica isolates (S. Typhimurium, S. Enteriditis, S. Infantis, S. Kentucky and S. Heidelberg). There was a significant increase in the prevalence rates of blaCTX-M (32.4%) and blaSHV-12 (14.7%) recorded in this study and those of blaCTX-M (11.3%) and blaSHV-12 (7.5%) previously reported in retail meats collected in 2010 in Egypt [17] (Figure 3, Supplementary Table S4). Recently, 2.7% of S. enterica isolates in chicken meat in Bangladesh were positive for blaCTX-M-1 [15]. Similarly, blaCTX-M (3.2%) and blaSHV (4.8%) were detected in S. Heidelberg strains from the poultry production chain (poultry, poultry meat, and a poultry farm) in Brazil [16]. Furthermore, a recent report from Italy showed that 80.5% of S. Infantis isolates from a broiler food chain possessed the blaCTX-M-1 gene [13]. In the USA, 61% of S. Infantis isolates from the poultry production chain carried the blaCTX-M-65 gene [12]. In Russia, all MDR S. Infantis isolates from chicken food products carried the blaCTX-M-14 gene [30]. In South Korea, all ESBL-resistant S. Virchow in chicken carcass samples were positive for blaCTX-M-15 [31], and only 31.0% of ESBL-resistant S. Virchow and S. Enteritidis isolated from retail chicken meat were positive for blaCTX-M-15 and blaCTX-M-79 [23]. In China, the blaCTX-M-14 gene was found in an MDR S. Kentucky strain isolated from a poultry slaughterhouse [32], and more recently, the blaCTX-M-55 gene was detected in 2.4% of S. Enteritidis strains isolated from retail foods [22]. More recently, in the Thailand, Cambodia, Lao PDR, and Myanmar border area, the blaCTX-M-55 and blaCTX-M-14 genes were identified in ESBL-producing S. enterica (1.9%) and E. coli (6.3%) strains isolated from pigs and pork [33]. Notably, the predominant ESBL-encoding genes in Enterobacteriaceae isolated from raw chicken and sushi in Spain were blaSHV-12 (50.1%), and blaCTX-M (20.8%) [25]. Additionally, more recently, we have identified blaCTX-M-3, blaCTX-M-14, blaCTX-M-15, blaSHV-1, blaSHV-2, and blaSHV-12 in S. enterica isolated from retail fishes in Egypt [26]. Interestingly, recently in Japan, ESBL-producing S. enterica isolates carrying blaCTX-M-15 or blaCTX-M-14 genes were identified in the stool samples of healthy food workers from several restaurants and food factories [34]. Therefore, food workers act as a reservoir of ESBL-producing S. enterica and may contribute to the spread of these dangerous bacteria via food products of animal origin. It is worth mentioning that, more recently in Peru, an MDR S. Infantis clone carrying blaCTX-M-65 and causing diarrhea in children has been disseminated between retail chicken meat and children [35]. Therefore, there is also a possibility of the dissemination of MDR S. enterica strains (carrying ESBL-and PMQR genes) between retail meats and humans in Egypt, and therefore, it is considered a major threat to public health.

3.3. High Prevalence of Plasmid-Mediated Quinolone Resistance Genes in S. enterica Isolated from Retail Meats and Beef Carcasses in Egypt

Fluoroquinolones are widely used in human and veterinary practices worldwide to treat bacterial diseases. Therefore, S. enterica with resistance or reduced susceptibility to fluoroquinolones is of serious concern, as these compounds are among the first choice of antimicrobials for the treatment of invasive and systemic salmonellosis in humans and animals [36,37]. The plasmid-mediated quinolone resistance (PMQR) genes confer decreased susceptibility to fluoroquinolones and enhance a high level of fluoroquinolone resistance in association with chromosomal mutations in DNA gyrase and topoisomerase IV genes [38]. The most common PMQR genes among Gram-negative bacteria are qnrA, qnrB, qnrS, and aac(6′)-Ib-cr [38]. The contribution of plasmid-mediated quinolone resistance (PMQR) genes in the emergence and spread of fluoroquinolones resistance among S. enterica is well-documented worldwide. In our study, the prevalence of PMQR genes from retail meats was significantly higher (67.6%) than that (28.3%) reported from our previous study on S. enterica isolates collected in 2010 from Egypt [17] (Figure 3, Supplementary Table S3). In the current study, PMQR genes: qnrA, qnrB, qnrS, and aac(6′)-Ib-cr were found at high prevalence rates: 5.9%, 23.5%, 35.3%, and 20.6%, respectively, compared with low prevalence rates: 1.9%, 11.2%, 5.7%, and 20.6%, respectively, reported in our previous study [17] (Figure 3, Supplementary Table S3). Notably, the occurrence of PMQR genes in S. enterica isolates from retail meats varies greatly worldwide. In Bangladesh, the prevalence of qnrA and qnrS genes in S. enterica from chicken meat was 4.1 and 6.8%, respectively [15]. In Chile, qnrB was detected in 2.3% of S. Infantis isolates from chicken meat [14]. In the USA, there was a significantly high prevalence rate (90%) of PMQR genes in S. enterica isolates from swine cecal contents and retail pork products, and the prevalence rates of qnrB and qnrS genes were 80% and 6.7%, respectively [39]. More recently, in China, the qnrS gene was detected in 0.8% of S. Enteritidis strains isolated from retail foods [22].

3.4. Common Plasmid Replicon Types in S. enterica Isolated from Retail Meat and Beef Carcasses in Egypt

Plasmids play an important role in the horizontal transfer of antimicrobial-resistance genes in Gram-negative bacteria including S. enterica. In our study, molecular analysis of plasmid transferability and replicon typing indicated that most plasmids (including ESBL-encoding genes and PMQR genes) are transferrable. PCR-based replicon typing showed that IncI1, IncA/C, IncN, IncHI1, and IncHI2 were the most common incompatibility groups (Supplementary Table S5). These incompatibility-group types were previously identified in plasmids among different ESBL and PMQR-producing S. enterica worldwide [17,26,40,41,42,43]. It is well known that these plasmid-incompatibility groups play a crucial role in the spread and dissemination of many antimicrobial resistance genes, particularly ESBL-encoding genes in Gram-negative bacteria [44]. Notably, in the USA, the IncI1 and IncA/C plasmids were responsible for the transfer and dissemination of the extended-spectrum cephalosporin resistance among S. Heidelberg from chicken meat to humans [45].

4. Materials and Methods

4.1. Sample Collection

A total of 400 samples (160 chicken meat, 120 beef meat, and 120 beef carcass swabs) were randomly collected from different street vendors, butchers, retail markets, and slaughterhouses in 38 cities from four governorates (Dakahlia, Damietta, Gharbia, and Kafr El-Sheikh) in Egypt, between January and September 2020 (details of samples sources and locations are present in Supplementary Tables S6 and S7). Samples were collected in sterile bags and labeled, then transferred in boxes with ice and examined immediately after arrival at the laboratory.

4.2. Isolation and Identification of S. enterica

Salmonella isolation was carried out by a standard cultivation method as recommended by ISO 6579-1 [46]. Samples (25 g meat or a swab pre-moistened with 25 mL buffered peptone water, Oxoid, UK) were inserted in stomacher bags containing buffered peptone water (225 mL). The homogenization was carried out at 320 rpm for 2 min, followed by incubation at 37 °C overnight. Then, 0.1 mL aliquots were inoculated into tubes containing 10 mL Rappaport Vassiliadis (RV) broth (Oxoid, UK) and then, incubated at 42 °C for 48 h. Then, XLD (xylose lysine deoxycholate) agar (Oxoid, UK) plates were inoculated from each of the RV broths and incubated at 37 °C for 18–24 h. Suspect colonies of Salmonella were biochemically confirmed using the API 20E system (bioMérieux, Marcy-l’Étoile, France). Then, Salmonella isolates were serotyped by using specific Salmonella O and H agglutinating antisera (Difco, Sparks, MD, USA) according to the Kauffman–White serotyping scheme [47]. Of note, local S. enterica strains isolated from retail meat and dairy products in Egypt were used as controls for the experiments [17].

4.3. Antimicrobial Sensitivity Testing and ESBL-Resistance Phenotyping

The Kirby–Bauer disk diffusion assay was used for the determination of antimicrobial-sensitivity phenotypes of bacterial isolates according to the standards and interpretive criteria described by the Clinical and Laboratory Standards Institute [48]. The types of antibiotics used are present in Figure 2. The disks were purchased from Oxoid, UK, and the results were recorded based on CLSI guidelines [48]. Escherichia coli ATCC 25922 was used as quality control. For the detection of the ESBL-resistance phenotype, the double-disc synergy test was used. Briefly, pairs of disks containing ceftazidime (CAZ), 30 µg, and cefotaxime (CTX), 30 µg, were used with and without amoxicillin–clavulanic acid (AMC) 20/10 μg on the same inoculated plate containing Muller-Hinton agar (Oxoid, UK). A positive test result was defined as a 5 mm increase in the zone diameter compared to that of a disk without clavulanic acid [49].

4.4. Preparation of Salmonella DNA

Salmonella DNA was prepared using boiled lysates, as previously described [17]. Salmonella colonies were subcultured in LB broth. Then, 200 μL of overnight bacterial culture was mixed with 800 μL of distilled water and boiled for 10 min. The resulting solution was centrifuged, and the supernatant was used as the DNA template and stored until use at −20 °C.

4.5. PCR and DNA Sequencing for β-Lactamase-Encoding Genes and Plasmid-Mediated Quinolone Resistance Genes

Screening for TEM, SHV, CTX-M, OXA, and CMY β-lactamase-encoding genes was performed by PCR using universal primers for the TEM, SHV, OXA, CTX-M, and CMY families, as described previously [50]. Screening for IMP, NDM, SPM, VIM, and OXA-48 carbapenemase-encoding genes was performed using multiplex PCR as described previously [51]. Finally, PCR amplification was used to screen for plasmid-mediated quinolone-resistance genes, qnrA, qnrB, qnrS and aac(6′)-Ib-cr, using previously described primers [50]. The PCR amplicons were subjected to electrophoresis in a 1.0% agarose gel, stained with ethidium bromide, and visualized under ultraviolet light. Then, PCR fragments were purified using a QIAquick Gel Extraction Kit (Qiagen, Tokyo, Japan) from the agarose gel. An ABI automatic DNA sequencer (Model 373; Perkin-Elmer, Waltham, MA, USA) was used for sequencing both strands of the PCR products. Primers are compiled in Supplementary Table S8. Local S. enterica strains isolated from retail meat and dairy products in Egypt and carrying resistance genes were used as controls for the experiments [17].

4.6. Plasmid Incompatibility Grouping and Transconjugation Experiments

The mating-out assay was used for the determination of the transferability of plasmids using S. enterica isolates as donors and a rifampicin-resistant mutant of E. coli HB101 as the recipient, as described previously [17]. Transconjugants were selected on agar supplemented with AMP (100 mg/L) and rifampicin (250 mg/L). Plasmid DNA was extracted from both S. enterica isolates and E. coli transconjugants using the Kado and Liu method [52]. PCR-based replicon typing was used for the determination of plasmid incompatibility grouping, as previously described [53]. PCR assays on the transconjugants were used for the confirmation of the transfer of resistance genes, as described previously [17]. Primers are compiled in Supplementary Table S8. Local S. enterica strains isolated from retail meat and dairy products in Egypt and carrying plasmid replicon types were used as controls for the experiments [17].

4.7. BLAST Analysis of the Sequence Data

The BLAST program (available at the NCBI BLAST homepage: http://blast.ncbi.nlm.nih.gov/Blast.cgi; accessed on 19 July 2021) was used for carrying out a similarity search for DNA sequencing data.

5. Conclusions

Our study highlights the role of retail meats as a potential source for MDR S. enterica strains carrying ESBL and PMQR genes. This is considered a potential public health threat that requires urgent attention from health professionals to ensure food safety in Egypt. Additionally, these findings emphasize the importance of continuous monitoring to track the emergence and changes in antibiotic resistance in the food chain in Egypt by ongoing surveillance in the future.

Supplementary Materials

The following are available online at https://www.mdpi.com/article/10.3390/antibiotics10070881/s1 Table S1: Prevalence of Salmonella enterica serovars isolated from retail meats and slaughterhouses. Table S2: Resistance phenotypes of Salmonella enterica isolated from retail meats and slaughterhouses. Table S3: The sources of resistance phenotypes of Salmonella enterica isolated from retail meats and beef carcasses in Egypt. Table S4: Comparison between the prevalence rates of resistance phenotypes and genes in Salmonella enterica isolated from retail meats and slaughterhouses in 2010 and 2020 from Egypt. Table S5: Results of conjugation experiments and plasmid replicon typing for Salmonella enterica isolated from retail meats and beef carcasses in Egypt. Table S6: Numbers and sources of meat samples used in this study. Table S7: City names and numbers of meat samples collected from four governorates (Dakahlia, Damietta, Gharbia, and Kafr El-Sheikh) in Egypt. Table S8: Primers used for PCR and DNA sequencing.

Author Contributions

Conceptualization, A.M.A. and T.S.; methodology, W.A.A., A.M.A. and Y.H.; writing—original draft preparation, A.M.A.; writing—review and editing, A.M.A., Y.H., H.A.T. and T.S. All authors have read and agreed to the published version of the manuscript.

Funding

This work was partially funded by a young researcher grant to A.M.A. from the Science and Technology Development Fund (STDF), Ministry of Higher Education, Egypt, project number 540.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The authors confirm that the data that support the findings of this study are available within the article.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Prevalence of different Salmonella enterica serovars isolated from retail chicken meat, beef meat, and beef carcasses in Egypt.
Figure 1. Prevalence of different Salmonella enterica serovars isolated from retail chicken meat, beef meat, and beef carcasses in Egypt.
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Figure 2. Resistance phenotypes of Salmonella enterica isolated from retail chicken meat, beef meat, and beef carcasses in Egypt. AMC, amoxicillin-clavulanic acid; AMP, ampicillin; ATM, aztreonam; CHL, chloramphenicol; CIP, ciprofloxacin; CAZ, ceftazidime; CPD, cefpodoxime; CRO, ceftriaxone; CTT, cefotetan; CTX, cefotaxime; ESBL, extended-spectrum β-lactamase; FOX, cefoxitin; GEN, gentamicin; NAL, nalidixic acid; OXA, oxacillin; STR, streptomycin; SXT, sulfamethoxazole-trimethoprim; TET, tetracycline.
Figure 2. Resistance phenotypes of Salmonella enterica isolated from retail chicken meat, beef meat, and beef carcasses in Egypt. AMC, amoxicillin-clavulanic acid; AMP, ampicillin; ATM, aztreonam; CHL, chloramphenicol; CIP, ciprofloxacin; CAZ, ceftazidime; CPD, cefpodoxime; CRO, ceftriaxone; CTT, cefotetan; CTX, cefotaxime; ESBL, extended-spectrum β-lactamase; FOX, cefoxitin; GEN, gentamicin; NAL, nalidixic acid; OXA, oxacillin; STR, streptomycin; SXT, sulfamethoxazole-trimethoprim; TET, tetracycline.
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Figure 3. Comparison between the prevalence rates of resistance phenotypes and genes in Salmonella enterica isolated from retail meats and beef carcasses in 2010 and 2020 in Egypt.
Figure 3. Comparison between the prevalence rates of resistance phenotypes and genes in Salmonella enterica isolated from retail meats and beef carcasses in 2010 and 2020 in Egypt.
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Table
Table 1. Resistance phenotypes and incidence of resistance genes in Salmonella enterica isolated from retail meats and beef carcasses in Egypt.
Table 1. Resistance phenotypes and incidence of resistance genes in Salmonella enterica isolated from retail meats and beef carcasses in Egypt.
No.IsolateSerovarSourceResistance PhenotypeESBL PhenotypeResistance Gene(s)
1SI-CM1S. InfantisChicken meatAMC, AMP, ATM, CAZ, CHL, CIP, CPD, CRO, CTT, CTX, FOX, GEN, NAL, OXA, STR, SXT, TET+blaTEM-1, blaCTX-M-1, blaCMY-2, blaOXA-1, qnrB, aac(6′)-Ib-cr
2SI-CM2S. InfantisChicken meatAMC, AMP, ATM, CHL, CPD, CTT, CTX, FOX, GEN, OXA, STR, SXT, TET+blaTEM-1, blaSHV-12
3SI-CM3S. InfantisChicken meatAMC, AMP, ATM, CAZ, CHL, CPD, CTT, CTX, FOX, GEN, OXA, STR, SXT, TET+blaTEM-1, blaCTX-M-14, blaCMY-2
4SI-CM4S. InfantisChicken meatAMP, CHL, CTT, FOX, OXA, STR, TET-blaOXA-1
5SI-CM5S. InfantisChicken meatAMP, CHL, CIP, NAL, STR, TET-blaTEM-1, qnrS
6SI-CM6S. InfantisChicken meatAMC, AMP, ATM, CTT, FOX, GEN, OXA, STR, SXT, TET-blaCMY-2
7SI-BM1S. InfantisBeef meatAMP, ATM, CTT, FOX, OXA, STR, SXT, TET-blaTEM-1
8SI-BC1S. InfantisBeef carcassAMP, CHL, NAL, STR-blaTEM-1, qnrB
9SI-BC2S. InfantisBeef carcassAMP, CTT, FOX, OXA, STR-blaOXA-1
10SI-BC3S. InfantisBeef carcassAMP, NAL-blaTEM-1, qnrS
11ST-CM1S. TyphimuriumChicken meatAMC, AMP, ATM, CAZ, CHL, CIP, CPD, CRO, CTT, CTX, FOX, GEN, NAL, OXA, STR, SXT, TET+blaTEM-1, blaCTX-M-15, blaCMY-2, blaOXA-1, qnrB, aac(6′)-Ib-cr
12ST-CM2S. TyphimuriumChicken meatAMC, AMP, ATM, CAZ, CHL, CIP, CPD, CTT, CTX, FOX, GEN, NAL, OXA, STR, SXT, TET+blaTEM-1, blaCTX-M-3, blaSHV-12, qnrB
13ST-BM1S. TyphimuriumBeef meatAMC, AMP, ATM, CHL, CTT, FOX, OXA, STR, SXT, TET-blaTEM-1
14ST-BM2S. TyphimuriumBeef meatAMC, AMP, ATM, CAZ, CHL, CIP, CPD, CRO, CTT, CTX, FOX, GEN, NAL, OXA, STR, SXT, TET+blaTEM-1, blaCTX-M-14, blaOXA-1, qnrS
15ST-BC1S. TyphimuriumBeef carcassAMC, AMP, ATM, CAZ, CHL, CPD, CTT, CTX, FOX, GEN, NAL, OXA, STR, SXT, TET+blaTEM-1, blaCTX-M-13, qnrS
16ST-BC2S. TyphimuriumBeef carcassAMP, OXA, CHL, NAL, STR-blaTEM-1, qnrA
17ST-BC3S. TyphimuriumBeef carcassAMP, ATM, CHL, CTT, FOX, GEN, NAL, OXA, STR, SXT, TET-blaTEM-1, qnrS
18SE-CM1S. EnteritidisChicken meatAMC, AMP, ATM, CAZ, CHL, CIP, CPD, CRO, CTT, CTX, FOX, GEN, NAL, OXA, STR, SXT, TET+blaTEM-1, blaCTX-M-3, blaCMY-2, blaOXA-1, qnrB, aac(6′)-Ib-cr
19SE-CM2S. EnteritidisChicken meatAMC, AMP, ATM, CAZ, CHL, CPD, CTT, CTX, FOX, GEN, NAL, OXA, STR, SXT, TET+blaTEM-1, blaCTX-M-15, qnrS
20SE-CM3S. EnteritidisChicken meatAMC, AMP, ATM, CHL, CTT, CTX, FOX, NAL, OXA, STR, SXT TET+blaTEM-1, blaSHV-12, qnrS
21SE-BC1S. EnteritidisBeef carcassAMP, ATM, CTT, FOX, OXA, STR-blaOXA-1, blaCMY-2
22SV-CM1S. VirchowChicken meatAMC, AMP, ATM, CAZ, CHL, CPD, CRO, CTT, CTX, FOX, GEN, NAL, OXA, STR, SXT, TET+blaTEM-1, blaCTX-M-15, aac(6′)-Ib-cr
23SV-BM1S. VirchowBeef meatAMP, CHL, CTT, GEN, NAL, OXA, STR, SXT, TET-blaTEM-1, qnrS
24SV-BC1S. VirchowBeef carcassAMC, AMP, ATM, CHL, CTT, FOX, GEN, OXA, STR, SXT, TET-blaTEM-1, blaOXA-1, blaCMY-2
25SV-BC2S. VirchowBeef carcassAMP, NAL, CHL-qnrB
26SH-CM1S. HeidelbergChicken meatAMC, AMP, ATM, CAZ, CHL, CIP, CPD, CRO, CTT, FOX, GEN, NAL, OXA, STR, SXT, TET+blaTEM-1, blaCTX-M-2, blaCMY-2, blaSHV-12, qnrB
27SH-CM2S. HeidelbergChicken meatAMP, ATM, CHL, CTT, FOX, GEN, OXA, STR, SXT, TET-blaTEM-1, blaCMY-2
28SH-CM3S. HeidelbergChicken meatAMP, OXA, NAL, TET-blaTEM-1, qnrB
29SK-CM1S. KentuckyChicken meatAMC, AMP, CAZ, CHL, CIP, CPD, CRO, CTT, CTX, FOX, GEN, NAL, OXA, STR, SXT, TET+blaTEM-1, blaCTX-M-15, blaCMY-2, blaOXA-1, qnrS, aac(6′)-Ib-cr
30SK-CM2S. KentuckyChicken meatAMC, AMP, ATM, CHL, CIP, CTT, CTX, FOX, GEN, NAL, OXA, STR, SXT, TET+blaTEM-1, blaSHV-12, aac(6′)-Ib-cr
31SAN-CM1S. AnatumChicken meatAMP, CHL, CTT, NAL, OXA, STR, SXT, TET-blaOXA-1, qnrS
32SAG-CM1S. AgonaChicken meatNAL-qnrA
33SM-BC1S. MontevideoBeef carcassAMP, ATM, CHL, CTT, GEN, NAL, OXA, STR, SXT, TET-blaTEM-1, qnrS
34SS-BC1S. StanleyBeef carcassNAL, TET-qnrS
Table
Table 2. Prevalence of resistance genes in Salmonella enterica serovars isolated from retail meats and beef carcasses in Egypt.
Table 2. Prevalence of resistance genes in Salmonella enterica serovars isolated from retail meats and beef carcasses in Egypt.
S. enterica SerovarB-Lactamases Resistance GenesPlasmid-Mediated Quinolone Resistance Genes
ESBL-Type (No.)Narrow-Spectrum Types (No.)AmpC
(blaCMY)
(No.)		qnrAqnrBqnrSaac(6′)-Ib-cr
blaCTX-MblaSHVblaTEMblaOXA
InfantisblaCTX-M-1 (1) blaCTX-M-14 (1)blaSHV-12 (1)blaTEM-1 (7)blaOXA-1 (3)blaCMY-2 (3)-221
TyphimuriumblaCTX-M-3 (1) blaCTX-M-13 (1) blaCTX-M-14(1) blaCTX-M-15 (1)blaSHV-12 (1)blaTEM-1 (7)blaOXA-1 (2)blaCMY-2 (1)1232
EnteritidisblaCTX-M-3 (1) blaCTX-M-15 (1)blaSHV-12 (1)blaTEM-1 (3)blaOXA-1 (2)blaCMY-2 (1)-121
VirchowblaCTX-M-15 (1)-blaTEM-1 (3)blaOXA-1 (1)blaCMY-2 (1)-111
HeidelbergblaCTX-M-2 (1)blaSHV-12 (1)blaTEM-1 (3)-blaCMY-2 (2)-2--
KentuckyblaCTX-M-15 (1)blaSHV-12 (1)blaTEM-1 (2)blaOXA-1 (1)blaCMY-2 (1)--12
Anatum---blaOXA-1 (1)---1-
Agona-----1---
Montevideo--blaTEM-1 (2)----1-
Stanley-------1-
Total11 (32.4%)5 (14.7%)27 (79.4%)10 (29.4%)9 (26.5%)2 (5.9%)8 (23.5%)12 (35.3%)7 (20.6%)
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Adel, W.A.; Ahmed, A.M.; Hegazy, Y.; Torky, H.A.; Shimamoto, T. High Prevalence of ESBL and Plasmid-Mediated Quinolone Resistance Genes in Salmonella enterica Isolated from Retail Meats and Slaughterhouses in Egypt. Antibiotics 2021, 10, 881. https://doi.org/10.3390/antibiotics10070881

AMA Style

Adel WA, Ahmed AM, Hegazy Y, Torky HA, Shimamoto T. High Prevalence of ESBL and Plasmid-Mediated Quinolone Resistance Genes in Salmonella enterica Isolated from Retail Meats and Slaughterhouses in Egypt. Antibiotics. 2021; 10(7):881. https://doi.org/10.3390/antibiotics10070881

Chicago/Turabian Style

Adel, Wesam A., Ashraf M. Ahmed, Yamen Hegazy, Helmy A. Torky, and Tadashi Shimamoto. 2021. "High Prevalence of ESBL and Plasmid-Mediated Quinolone Resistance Genes in Salmonella enterica Isolated from Retail Meats and Slaughterhouses in Egypt" Antibiotics 10, no. 7: 881. https://doi.org/10.3390/antibiotics10070881

APA Style

Adel, W. A., Ahmed, A. M., Hegazy, Y., Torky, H. A., & Shimamoto, T. (2021). High Prevalence of ESBL and Plasmid-Mediated Quinolone Resistance Genes in Salmonella enterica Isolated from Retail Meats and Slaughterhouses in Egypt. Antibiotics, 10(7), 881. https://doi.org/10.3390/antibiotics10070881

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