Skip to main content

Prevalence of extended-spectrum β-lactamase-producing Enterobacterales in retail sheep meat from Zagazig city, Egypt

Abstract

Background

The goal of this study was to investigate the prevalence of extended-spectrum β-lactamase production in Enterobacterales isolated from retail sheep meat in Zagazig, Egypt.

Methods

One hundred random samples of sheep meat were collected from different retail butcher shops (n = 5) in the city of Zagazig, Egypt. Bacterial isolates were identified by MALDI-TOF MS and screened for antibiotic susceptibility by disk diffusion; further genotypic characterization of β-lactamase-encoding genes was performed with Real-Time PCR. E. coli strains were phylotyped with the Clermont triplex PCR method.

Results

Of the total of 101 bacterial isolates recovered from retail sheep meat samples, 93 were E. coli, six were Enterobacter cloacae and two were Proteus mirabilis. As many as 17% of these 100 samples showed ESBL phenotypes, all were E. coli. The blaCTX-M genes were detected in seven isolates (six were blaCTX-M-15 and one was blaCTX-M-14), three isolates harboured blaTEM (all were blaTEM-one), and two carried genes of the blaSHV family (both were blaSHV-12). Eight E. coli isolates expressed ESBL phenotype but no blaTEM, blaSHV or blaCTX-M genes were detected by PCR. ESBL- positive E. coli isolates were nearly equally distributed over the commensal groups A/B1 and the virulent group D.

Conclusion

Nearly one in five sheep meat samples was contaminated with ESBL-E. coli. This further corroborates the potential role played by contaminated meat in the increasing resistance rates that have been reported worldwide.

Peer Review reports

Background

Since the breakthrough discovery of penicillin in the 1928s, β-lactam antibiotics have saved countless lives, but it didn't take long for β-lactam-resistant bacteria to be identified [1]. The production of β-lactamases by enzymatic hydrolysis of the β-lactam ring is the primary contributor to β-lactam resistance [2]. Extended-spectrum beta-lactamases (ESBLs) are of particular concern among these enzymes because they inactivate extended-spectrum cephalosporins [3]. These enzymes can be produced by a wide range of bacteria, including Enterobacterales and non-fermenting bacteria [3,4,5]. Escherichia coli is the most common ESBL-producing species, and it frequently causes urinary tract infections, pneumonia, and even sepsis in humans [6].

According to recent studies, animals may serve as a reservoir for these ESBL-producing Enterobacterales [7,8,9]. The possibility that these antimicrobial-resistant Enterobacterales of animal origin are transmitted to humans via the food chain has been considered [10]. Furthermore, evidence of a link between antimicrobial use in food-producing animals and human resistance has been reported [11].

The contamination of raw meats with ESBL-producing Enterobacterales (ESBL-E) is a growing problem because they play a potential role in the spread of ESBL genes to humans via food chains [12]. ESBL-E contamination of raw retail meats has been detected in studies all over the world [13,14,15,16]. In Egypt, the national antimicrobial stewardship program has been established but there are no strict laws to enforce its implementation [17, 18]. Antimicrobials such as tetracycline, quinolones, and beta lactams are still used in Egypt for animal feed growth promotion and by veterinarians to treat and prevent zoonotic diseases [19]. There is a scarcity of data on ESBL-producing bacteria in Egyptian food animals. In a previous study, we discovered that ESBL-E was present in 63% of Egyptian retail chicken meat samples [9]. Because of the high ESBL-E contamination rate, the aim of this current study was to determine the prevalence of ESBL-E in retail sheep meat from Zagazig, Egypt.

Results

Out of 100 retail sheep meat samples, 101 enterobacterial isolates were recovered, 93 were E. coli, six were Enterobacter cloacae and two were Proteus mirabilis. Putative ESBL-E isolates were identified in 17 samples (Table 1). All isolates with ESBL phenotype belonged to E. coli. All isolates were susceptible to meropenem and imipenem (Fig. 1).

Table 1 Enterobacterales strains isolated from 100 retail sheep meat samples collected from Zagazig, Egypt
Fig. 1
figure 1

Overview of antimicrobial resistance pattern. Antimicrobial resistant genes of all Enterobacterales strains isolated from 100 retail sheep meat collected from Zagazig city, Egypt

blaCTX-M were identified in 41.18% (7/17) of the ESBL-producing E. coli, whereas blaTEM and blaSHV were detected in 17.65% (3/17) and 11.76% (2/17), respectively. Concomitant presence of blaCTX-M and blaTEM was detected in 3 isolates, 4 isolates expressed blaCTX-M alone, and 2 harboured only blaSHV. Eight E. coli isolates expressed ESBL phenotype but no blaTEM, blaSHV or blaCTX-M genes were detected by PCR (Table 2).

Table 2 Characteristics of ESBL-producing E. coli strains isolated from 100 retail sheep meat collected from Zagazig, Egypt

Of the seven blaCTX-M – positive E. coli isolates, six (85.7%) were blaCTX-M-15 positive, and one blaCTX-M-14. All the three TEM genes were blaTEM-one while the two blaSHV-type ESBL genes were identified as blaSHV-12.

Disc-diffusion antimicrobial susceptibility testing revealed that of 17 ESBL-producing isolates, 13 (76.47%) were resistant to trimethoprim/sulfamethoxazole, 9 (52.94%) to aminoglycosides, 6 (35.29%) to quinolones, and only one to nitrofurantoin, while 5 (29.41%) were multidrug resistant (resistant to three or more antimicrobial classes) (Fig. 2).

Fig. 2
figure 2

Antimicrobial resistance profile of E. coli strains isolated from 100 retail sheep meat collected from Zagazig, Egypt (ESBL, extended-spectrum beta-lactamases; AM, aminoglycosides; TS, trimethoprim/sulfamethoxazole; NIT, nitrofurantoin; QU, quinolones)

Phylogenetic grouping of 17 ESBL-positive E. coli isolates showed that six isolates belonged to group A, two to group B1, nine to group D, while no isolates belonged to group B2. The 76 ESBL-negative isolates were: 27 group A, 46 group B1, one group B2 and two group D (Table 2).

Discussion

Extended-spectrum β-lactamase-producing bacteria are one of the fastest emerging resistance problems worldwide [15]. Livestock may be an important vehicle for the community-wide dissemination of ESBL-producing bacteria [7]. In Egypt, the role of food-producing animals has not been fully assessed; nothing is known about possible contamination of sheep meat with ESBL-producing Enterobacterales and their encoding genes. Our study showed that all retail meat samples were contaminated with Enterobacterales; of these over 90% was E. coli. The frequency of E. coli among contaminating Enterobacterales coincides with what has been described earlier in other studies [20,21,22].

This study revealed that nearly one in five E. coli isolates was ESBL positive, showing that also sheep meat may be a source of ESBL-producing strains for humans. Sheep meat, however, appeared less contaminated than chicken meat in Egypt. We have shown previously that in the same region in Egypt, over 65% of retail chicken meat samples were positive for ESBL-E [9]. Possibly, the difference in contamination rates between chicken and sheep meat owes to differences in the production system, which is more intensive in poultry industry than in the sheep rearing system [23,24,25]. In our study, the frequency of ESBL-producing E. coli was higher to that reported for sheep meat in Switzerland (8.6%) [26] and Portugal (5.5%) [27], while it was lower than the 60% reported in Iran [28], 63.8% detected in chicken meat in Tunisia [29], 27.5% found in ground beef samples in Algeria [30] and 23% identified among imported chicken meat in Gabon [31]. The difference in prevalence of ESBL-E between these countries could be attributed to poor antibiotic use regulations in Middle East unlike the restricted policy of antibiotic use adopted by EU countries [32].

In this study, various types of ESBL-encoding genes were identified including blaCTX-15, blaCTX-14, blaTEM-one and blaSHV-12. Our results are similar to those of a previous report from Egypt, in which blaCTX, blaTEM and blaSHV were found in ESBL-producing E. coli recovered from meat and dairy farms [9, 33]. However, the occurrence of β-lactamase genes in our study is higher than in recent reports from Turkey [34], Switzerland [26], Portugal [27] and Japan [35]. Regarding the types of blaCTX-M gene, our data showed that blaCTX-M-15 was the most frequent ESBL-type in our E. coli collection. This is consistent with our finding that blaCTX-M-15 was also the most frequent ESBL in E. coli from chicken meat in Egypt. In other countries, e.g. Switzerland and Portugal, blaCTX-M-14 appeared as the most prevalent gene in E. coli isolates from sheep meat [26, 27] while in Gabon, Tunisia and Algeria the blaCTX-M-one was predominant in ESB-E. coli from meat samples [29,30,31]. Eight E. coli showed ESBL phenotype, but they were negative for screened ESBL genes, this could be attributed to production of unscreened minor ESBL genes as OXA-type beta lactamases.

In the present study, the ESBL-producing E. coli isolates showed high frequency of co-resistance to trimethoprim/sulfamethoxazole, aminoglycosides, quinolones and nitrofurantoin, which is similar to other reports on antimicrobial resistance of E. coli isolates recovered from retail meat in Egypt [9, 33], China [22], Turkey [36], and Italy [37]. This multi-resistance trait showed that nearly 40% (n = 5) of the isolates were multidrug resistant (MDR). Similarly, high levels of MDR isolates recovered from sheep meat [27], retail chicken meat [9], and beef meat [21] have been reported in Portugal, Egypt and Spain, respectively. The presence of a high level of MDR isolates could be related to the unrestricted usage of antibiotics in food animals and farms [25]. Phylogenetic grouping of ESBL positive E. coli revealed a uniform distribution of ESBL genes among virulent and avirulent phylogenetic groups, inconsistent with antibiotic resistance—virulence trade off hypothesis [38]. In addition, the distribution of phylogenetic groups may vary according to the geographic regions [39].

Conclusions

Our findings highlight the possible role played by contaminated sheep meat as a source of antibiotic-resistant bacteria in Egypt. The high prevalence of ESBL-producing multidrug-resistant Enterobacterales detected in retail sheep meat, increases the concern regarding human exposure to superbugs. Thus, to tackle antibiotic resistance in the human–animal interface, proactive efforts should be taken to establish national action plans based on the One Health approach [40].

Methods

Study area

This study was performed in Zagazig city, which is the capital of Sharkia governorate, Egypt. Zagazig city is located in the northern part of Egypt at latitude 30°35′15″ N; longitude 31°30′07″ E and altitude 16 m above sea level (Fig. 3). Sharkia governorate considered the third populous governorate in Egypt, has a strong an agriculture industry and has also a high density of ruminants (cattle, sheep and goats) which are used mainly for meat production.

Fig. 3
figure 3

Map of Egypt showed the location of Zagazig city (grey colour) in Sharkia governorate and the location of the five retail butcher shops in Zagazig city (red dots). The map was created using R software (R Core Team, 2019; version 3.5.3) and “cartography” and “sf” packages

Study design and sampling strategy

A cross-sectional study was performed from January 2013 to May 2013. The required number of sheep meat samples was determined using the formula for simple random sampling, with 10% expected prevalence, 5% absolute precision and 95% confidence interval. In total, 100 samples of sheep meat were collected from five retail butcher shops in Zagazig city. The shops were visited once bi-weekly. At each visit, two random meat samples were purchased from each shop, and immediately transported to the laboratory for culture.

Isolation and identification of Enterobacterales

Sampling was performed by swabbing–based method [41]. Each swab was immersed in 5 mL of physiological saline solution (0.9%), mixed well by vortexing for 10 s, centrifuged at 3,500 × g for 15 min, most of the supernatant was decanted and 100 µL of the sediment was inoculated directly on selective EbSA-ESBL Screening Agar [42] for the characterization of extended-spectrum cephalosporin-resistant Gram-negative bacteria and on MacConkey agar for the isolation of the dominant bacteria. A pure bacterial colony was picked up from both culture plates for further identification by the automated Vitek® MS system (BioMérieux, Marcy l’Étoile, France).

Phenotypic screening and confirmation of ESBL-E

Bacterial isolates were tested for antibiotic susceptibility by disk diffusion method on Mueller–Hinton agar using ceftazidime (30 μg), cefotaxime (30 μg), cefepime (30 μg), meropenem (10 μg), imipenem (10 μg), nitrofurantoin (100 μg), norfloxacin (10 μg), gentamicin (10 μg), and trimethoprim/sulfamethoxazole (1.25–23.75 µg) disks. Antibiotic inhibition zone diameters were evaluated in conformity with to CLSI–approved interpretive criteria [43]. Combination disks method was employed to confirm ESBL production, according to the guidelines of the Dutch Society of Medical Microbiology [44].

Genotypic characterization of β-lactamase-encoding genes

ESBL phenotypes were tested for genes encoding blaTEM, blaSHV and blaCTX-M by real-time PCR using primers described before [45,46,47]. Subsequently, sequencing was performed with the Sanger ABI 3730 XL automated DNA sequencer (BaseClear, Leiden, The Netherlands), and analysis was performed with the Codon Code Aligner software (Version 5.0.2). The obtained nucleotide sequences were compared with described sequences available at the National Center for Biotechnology Information website (www.ncbi.nlm.nih.gov).

E. coli phylotyping

Assignment of E. coli isolates to phylotypes (A, B1, B2 or D) was done based on the Clermont triplex PCR method targeting chuA, yjaA and the TspE4.C2 DNA fragment [48].

Data analysis

Information collected, and the antimicrobial resistance results were coded and entered into Microsoft Excel, and the descriptive statistical data analysis was performed using STATA version 15 for Windows (Stata Corp., USA). However, the heatmap was created using the R package “Complex-Heatmap” [49].

Availability of data and materials

The datasets generated and/or analysed during the current study are available in the [Figshare] repository, [https://figshare.com/articles/dataset/Raw_data_of_ESBL-E_in_retail_sheep_meat/19139714].

Abbreviations

E. coli :

Escherichia coli

PCR:

Polymerase chain reaction

ESBLs:

Extended-spectrum beta-lactamases

MDR:

Multidrug resistant

CLSI:

Clinical and laboratory standards institute

References

  1. Butler MS, Blaskovich MA, Cooper MA. Antibiotics in the clinical pipeline in 2013. J of Antibiot. 2013;66(10):571–91.

    CAS  Article  Google Scholar 

  2. Poole K. Resistance to β-lactam antibiotics. Cellular and Molecular Life Sciences CMLS. 2004;61(17):2200–23.

    CAS  PubMed  Article  Google Scholar 

  3. Rawat D, Nair D. Extended-spectrum β-lactamases in Gram Negative Bacteria. J Glob Infect Dis. 2010;2(3):263.

    PubMed  PubMed Central  Article  Google Scholar 

  4. Bradford PA. Extended-spectrum β-lactamases in the 21st century: characterization, epidemiology, and detection of this important resistance threat. Clin Microbiol Rev. 2001;14(4):933–51.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  5. Giamarellou H. Multidrug resistance in Gram-negative bacteria that produce extended-spectrum β-lactamases (ESBLs). Clin Microbiol Infect. 2005;11:1–16.

    CAS  PubMed  Article  Google Scholar 

  6. Abraham S, Chapman TA, Zhang R, Chin J, Mabbett AN, Totsika M, Schembri MA. Molecular characterization of Escherichia coli strains that cause symptomatic and asymptomatic urinary tract infections. J Clin Microbiol. 2012;50(3):1027–30.

    PubMed  PubMed Central  Article  Google Scholar 

  7. Carattoli A. Animal reservoirs for extended spectrum β-lactamase producers. Clin Microbiol Infect. 2008;14:117–23.

    PubMed  Article  Google Scholar 

  8. Overdevest I, Willemsen I, Rijnsburger M, Eustace A, Xu L, Hawkey P, Heck M, Savelkoul P, Vandenbroucke-Grauls C, van der Zwaluw K. Extended-spectrum β-lactamase genes of Escherichia coli in chicken meat and humans, The Netherlands. Emerg Infect Dis. 2011;17(7):1216.

    PubMed  PubMed Central  Article  Google Scholar 

  9. Abdallah H, Reuland E, Wintermans B, Al Naiemi N, Koek A, Abdelwahab A, Ammar A, Mohamed A, Vandenbroucke-Grauls C. Extended-spectrum β-lactamases and/or carbapenemases-producing Enterobacteriaceae isolated from retail chicken meat in Zagazig. Egypt PloS one. 2015;10(8):e0136052.

    CAS  PubMed  Article  Google Scholar 

  10. Aarestrup FM. Veterinary drug usage and antimicrobial resistance in bacteria of animal origin. Basic Clin Pharmacol Toxicol. 2005;96(4):271–81.

    CAS  PubMed  Article  Google Scholar 

  11. Angulo F, Nargund V, Chiller T. Evidence of an association between use of anti-microbial agents in food animals and anti-microbial resistance among bacteria isolated from humans and the human health consequences of such resistance. Zoonoses Public Health. 2004;51(8–9):374–9.

    CAS  Google Scholar 

  12. Blaak H, Hamidjaja RA, van Hoek AH, de Heer L, de Roda Husman AM, Schets FM. Detection of extended-spectrum beta-lactamase (ESBL)-producing Escherichia coli on flies at poultry farms. Appl Environ Microbiol. 2014;80(1):239–46.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  13. Borjesson S, Egervarn M, Lindblad M, Englund S. Frequent occurrence of extended-spectrum beta-lactamase-and transferable ampc beta-lactamase-producing Escherichia coli on domestic chicken meat in Sweden. Appl Environ Microbiol. 2013;79(7):2463–6.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  14. Voets GM, Fluit AC, Scharringa J, Schapendonk C, van den Munckhof T, Leverstein-van Hall MA, Stuart JC. Identical plasmid AmpC beta-lactamase genes and plasmid types in E. coli isolates from patients and poultry meat in the Netherlands. Int J Food Microbiol. 2013;167(3):359–62.

    CAS  PubMed  Article  Google Scholar 

  15. Petternel C, Galler H, Zarfel G, Luxner J, Haas D, Grisold AJ, Reinthaler FF, Feierl G. Isolation and characterization of multidrug-resistant bacteria from minced meat in Austria. Food Microbiol. 2014;44:41–6.

    CAS  PubMed  Article  Google Scholar 

  16. Le HV, Kawahara R, Khong DT, Tran HT, Nguyen TN, Pham KN, Jinnai M, Kumeda Y, Nakayama T, Ueda S. Widespread dissemination of extended-spectrum β-lactamase-producing, multidrug-resistant Escherichia coli in livestock and fishery products in Vietnam. Int J Food Contam. 2015;2(1):1–6.

    Article  Google Scholar 

  17. WHO: Egypt National Action Plan For Antimicrobial Resistance 2018–2022. https://www.who.int/publications/m/item/egypt-national-action-plan-for-antimicrobial-resistance. In.; 2018.

  18. El-Sokkary R, Kishk R, El-Din SM, Nemr N, Mahrous N, Alfishawy M, Morsi S, Abdalla W, Ahmed M, Tash R. Antibiotic Use and Resistance Among Prescribers: Current Status of Knowledge, Attitude, and Practice in Egypt. Infect Drug Resist. 2021;14:1209.

    PubMed  PubMed Central  Article  Google Scholar 

  19. WHO: Consultative Meeting on Antimicrobial Resistance for Countries in the Eastern Mediterranean Region: From Policies to Action [Online]. Sharm ElSheikh. Available online at: http://applications.emro.who.int/docs/IC_Meet_ep_2014_EN_15210.pdf. In.; 2013.

  20. Kola A, Kohler C, Pfeifer Y, Schwab F, Kühn K, Schulz K, Balau V, Breitbach K, Bast A, Witte W. High prevalence of extended-spectrum-β-lactamase-producing Enterobacteriaceae in organic and conventional retail chicken meat. Germany J Antimicrob Chemother. 2012;67(11):2631–4.

    CAS  PubMed  Article  Google Scholar 

  21. Ojer-Usoz E, González D, Vitas AI, Leiva J, García-Jalón I, Febles-Casquero A, de la Soledad EM. Prevalence of extended-spectrum β-lactamase-producing Enterobacteriaceae in meat products sold in Navarra. Spain Meat Sci. 2013;93(2):316–21.

    CAS  PubMed  Article  Google Scholar 

  22. Li L, Ye L, Kromann S, Meng H. Occurrence of extended-spectrum β-lactamases, plasmid-mediated quinolone resistance, and disinfectant resistance genes in Escherichia coli isolated from ready-to-eat meat products. Foodborne Pathog Dis. 2017;14(2):109–15.

    CAS  PubMed  Article  Google Scholar 

  23. Hughes L, Hermans P, Morgan K. Risk factors for the use of prescription antibiotics on UK broiler farms. J Antimicrob Chemother. 2008;61(4):947–52.

    CAS  PubMed  Article  Google Scholar 

  24. Smet A, Martel A, Persoons D, Dewulf J, Heyndrickx M, Herman L, Haesebrouck F, Butaye P. Broad-spectrum β-lactamases among Enterobacteriaceae of animal origin: molecular aspects, mobility and impact on public health. FEMS Microbiol Rev. 2010;34(3):295–316.

    CAS  PubMed  Article  Google Scholar 

  25. Dahshan H, Abd-Elall AMM, Megahed AM, Abd-El-Kader MA, Nabawy EE. Veterinary antibiotic resistance, residues, and ecological risks in environmental samples obtained from poultry farms. Egypt Environ Monit Assess. 2015;187(2):1–10.

    CAS  Article  Google Scholar 

  26. Geser N, Stephan R, Hächler H. Occurrence and characteristics of extended-spectrum β-lactamase (ESBL) producing Enterobacteriaceae in food producing animals, minced meat and raw milk. BMC Vet Res. 2012;8(1):1–9.

    Article  CAS  Google Scholar 

  27. Ramos S, Igrejas G, Silva N, Jones-Dias D, Capelo-Martinez J-L, Caniça M, Poeta P. First report of CTX-M producing Escherichia coli, including the new ST2526, isolated from beef cattle and sheep in Portugal. Food Control. 2013;31(1):208–10.

    CAS  Article  Google Scholar 

  28. Aliasadi S, Dastmalchi Saei H. Fecal carriage of Escherichia coli harboring extended-spectrum beta-lactamase (ESBL) genes by sheep and broilers in Urmia region. Iran Iran J Vet Res. 2015;9(2):93–101.

    Google Scholar 

  29. Hassen B, Abbassi MS, Ruiz-Ripa L, Mama OM, Hassen A, Torres C, Hammami S. High prevalence of mcr-1 encoding colistin resistance and first identification of blaCTX-M-55 in ESBL/CMY-2-producing Escherichia coli isolated from chicken faeces and retail meat in Tunisia. Int J Food Microbiol. 2020;318:108478.

    CAS  PubMed  Article  Google Scholar 

  30. Rebbah N, Messai Y, Chatre P, Haenni M, Madec JY, Bakour R. Diversity of CTX-M extended-spectrum β-lactamases in Escherichia coli isolates from retail raw ground beef: first report of CTX-M-24 and CTX-M-32 in Algeria. Microb Drug Resist. 2018;24(7):896–908.

    CAS  PubMed  Article  Google Scholar 

  31. Schaumburg F, Alabi AS, Frielinghaus L, Grobusch MP, Köck R, Becker K, Issifou S, Kremsner PG, Peters G, Mellmann A. The risk to import ESBL-producing Enterobacteriaceae and Staphylococcus aureus through chicken meat trade in Gabon. BMC Microbiol. 2014;14(1):1–7.

    Article  Google Scholar 

  32. Filippini M, Masiero G, Moschetti K. Socioeconomic determinants of regional differences in outpatient antibiotic consumption: evidence from Switzerland. Health Policy. 2006;78(1):77–92.

    PubMed  Article  Google Scholar 

  33. Braun SD, Ahmed MF, El-Adawy H, Hotzel H, Engelmann I, Weiß D, Monecke S, Ehricht R. Surveillance of extended-spectrum beta-lactamase-producing Escherichia coli in dairy cattle farms in the Nile Delta. Egypt Front Microbiol. 2016;7:1020.

    PubMed  Google Scholar 

  34. Tekiner İH, Özpınar H. Occurrence and characteristics of extended spectrum beta-lactamases-producing Enterobacteriaceae from foods of animal origin. Brazilian J Microbiol. 2016;47:444–51.

    CAS  Article  Google Scholar 

  35. Ahmed AM, Shimabukuro H, Shimamoto T. Isolation and molecular characterization of multidrug-resistant strains of Escherichia coli and Salmonella from retail chicken meat in Japan. J Food Sci. 2009;74(7):M405–10.

    CAS  PubMed  Article  Google Scholar 

  36. Pehlivanlar Önen S, Aslantaş Ö, Şebnem Yılmaz E, Kürekci C. Prevalence of β-lactamase producing Escherichia coli from retail meat in Turkey. J Food Sci. 2015;80(9):M2023–9.

    PubMed  Article  CAS  Google Scholar 

  37. Ghodousi A, Bonura C, Di Noto AM, Mammina C. Extended-spectrum ß-lactamase, AmpC-producing, and fluoroquinolone-resistant Escherichia coli in retail broiler chicken meat. Italy Foodborne Patho Dis. 2015;12(7):619–25.

    CAS  Article  Google Scholar 

  38. Johnson JR, Goullet P, Picard B, Moseley S, Roberts P, Stamm W. Association of carboxylesterase B electrophoretic pattern with presence and expression of urovirulence factor determinants and antimicrobial resistance among strains of Escherichia coli that cause urosepsis. Infect Immun. 1991;59(7):2311–5.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  39. Zhao R, Shi J, Shen Y, Li Y, Han Q, Zhang X, Gu G, Xu J. Phylogenetic distribution of virulence genes among ESBL-producing uropathogenic Escherichia coli isolated from long-term hospitalized patients. J Clin Diagn Res. 2015;9(7):DC01–4.

    PubMed  Google Scholar 

  40. Aslam B, Khurshid M, Arshad MI, Muzammil S, Rasool M, Yasmeen N, et al. Antibiotic Resistance: One Health One World Outlook. Front Cell Infect Microbiol. 2021;11:771510. https://doi.org/10.3389/fcimb.2021.771510.

  41. Pearce R, Bolton DJ. Excision vs sponge swabbing–a comparison of methods for the microbiological sampling of beef, pork and lamb carcasses. J Appl Microbiol. 2005;98(4):896–900.

    CAS  PubMed  Article  Google Scholar 

  42. Al Naiemi N, Murk J, Savelkoul P, Vandenbroucke-Grauls C, Debets-Ossenkopp Y. Extended-spectrum beta-lactamases screening agar with AmpC inhibition. Eur J Clin Microbiol Infect Dis. 2009;28(8):989–90.

    PubMed  PubMed Central  Article  Google Scholar 

  43. Cockerill FR, Wikler MA, Alder J, Dudley MN, Eliopoulos GM, Ferraro MJ, et al. Performance standards for antimicrobial susceptibility testing: twenty-second informational supplement. Clinical and Laboratory Standards Institute. 2012;32(3):M100–S22.

  44. Al Naiemi N, Cohen Stuart J, Leverstein van Hall M. NVMM Guideline Laboratory detection of highly resistant microorganisms (HRMO), version 2.0. 2012. Available: http://www.nvmm.nl/richtlijnen/hrmo-laboratorydetection-highly-resistant-microorganisms.

  45. Mulvey MR, Soule G, Boyd D, Demczuk W, Ahmed R. Characterization of the first extended-spectrum beta-lactamase-producing Salmonella isolate identified in Canada. J Clin Microbiol. 2003;41(1):460–2.

    PubMed  PubMed Central  Article  Google Scholar 

  46. Olesen I, Hasman H, Møller Aarestrup F. Prevalence of β-lactamases among ampicillin-resistant Escherichia coli and Salmonella isolated from food animals in Denmark. Microb Drug Resist. 2004;10(4):334–40.

    CAS  PubMed  Article  Google Scholar 

  47. Weill F-X, Demartin M, Tandé D, Espié E, Rakotoarivony I, Grimont PA. SHV-12-like extended-spectrum-β-lactamase-producing strains of Salmonella enterica serotypes Babelsberg and Enteritidis isolated in France among infants adopted from Mali. J Clin Microbiol. 2004;42(6):2432–7.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  48. Clermont O, Bonacorsi S, Bingen E. Rapid and simple determination of the Escherichia coli phylogenetic group. Appl Environ Microbiol. 2000;66(10):4555–8.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  49. Gu Z, Eils R, Schlesner M. Complex heatmaps reveal patterns and correlations in multidimensional genomic data. Bioinformatics. 2016;32(18):2847–9.

    CAS  PubMed  Article  Google Scholar 

Download references

Acknowledgements

This work was performed using the facilities of VU medical center, the Netherlands and we would like to thank the technicians for their excellent laboratory assistant.

Funding

Open access funding provided by The Science, Technology & Innovation Funding Authority (STDF) in cooperation with The Egyptian Knowledge Bank (EKB). This research received no specific grant from funding agencies.

Author information

Authors and Affiliations

Authors

Contributions

H.M.A. and I.E. analyze and wrote the main draft of the manuscript. H.M.A., N.A. and C.M.V. designed, planned and carried out the experiments. A.F.M. and G.A.S. performed sample collection. All authors read and approved the final manuscript.

Corresponding author

Correspondence to H. M. Abdallah.

Ethics declarations

Ethics approval and consent to participate

Ethical approval for animal research was not required as live animals were not used in this study.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Abdallah, H.M., Al Naiemi, N., Elsohaby, I. et al. Prevalence of extended-spectrum β-lactamase-producing Enterobacterales in retail sheep meat from Zagazig city, Egypt. BMC Vet Res 18, 191 (2022). https://doi.org/10.1186/s12917-022-03294-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s12917-022-03294-5

Keywords

  • ESBL
  • Antimicrobial
  • Egypt
  • Resistance