Prevalence, Characterization and PFGE profiles of multidrug resistance extended spectrum β-lactamase producing Escherichia coli strains in animal-derived food products from public markets in Eastern Turkey


Published: Nov 9, 2022
Updated: 2022-11-09
Keywords:
Escherichia coli Extended spectrum β-lactamase food MALDI-TOF MS PFGE
T Cebeci
https://orcid.org/0000-0001-8960-0587
Abstract
Multidrug-resistant (MDR) Extended-spectrum β-lactamase (ESBL)-producing Escherichia coli (E. coli) has increased markedly in recent years, which has currently posed a major challenge in antimicrobial treatments  and raised concerns regarding possible transfer of such bacteria through the food chain. The aim of this research was to investigate the prevalence of ESBL-producing E. coli in milk, cheese and meat samples and to determine their virulence, pathotype, serotype, antibiotic resistance and genetic relatedness. A total of 300 food samples  were purchased from public markets in different districts of Giresun city. Five (1.6%) of 300 food samples resulted positive for ESBL-producing E. coli isolation. β-Lactamase-encoding genes of the CTX-M (20%), TEM (40%), and SHV (20%) groups were detected singly or in combination. Five ESBL-producing E. coli isolates were further analysed for the presence of virulence genes. Virulence factor genes detected were hlyA (20%), ehlyA (20%), iutA (60%), iucD (40%), fimH (100%), kpsMTII (100%) and traT (100%). Of 130 E.coli isolates, 5 ESBL-producing E. coli strains (totally 3.8%) were isolated, including 3 EHEC (60%). No EIEC, ETEC, EPEC, DAEC or EAggEC3  was detected. In PCR, three stx2 (60%) and one flicH7 (20%) encoding genes were found in ESBL-producing E. coli isolates. In addition, genes encoding Shiga toxins were detected in 3 of 5 isolates, three isolates (60%) encoded O128 serotype.The antibiotic susceptibility test of positive isolates showed resistant to cefuroxime, trimethoprim/ sulfamethoxazole, cefazolin, streptomycin, ceftriaxone, tetracycline, ampicillin and trimethoprim. Most of ESBL-producing E. coli isolates showed 80% MDR phenotypes against at least four classes of antibiotics. Specific-PCR detection of antibiotic resistance genes showed the prevalence of the tetA gene in most of the isolates (80%), followed by dfrA, qnr, aadA1 and sul1. PFGE results show that the isolates from different districts presented no clonal relatedness. This is the first report of the characteristics of multidrug resistance ESBL-producing shigatoxigenic E. coli  in dairy and meat products in a local city in Turkey. Our findings indicate that dairy and meat products could be reservoirs of MDR ESBL-producing E. coli strains that were possessed several virulence factors and may be a cause of concern for human health.
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Author Biography
T Cebeci, Giresun University

Assistant Professor

References
Aibuedefe Osagie E (2019) Multiple Drug Resistance: A Fast-Growing Threat. Biomed J Sci Tech Res 21:. https://doi.org/10.26717/bjstr.2019.21.003572
Alegría Á, Arias-Temprano M, Fernández-Natal I, et al (2020) Molecular diversity of ESBL-producing Escherichia coli from foods of animal origin and human patients. Int J Environ Res Public Health 17:. https://doi.org/10.3390/ijerph17041312
Batabyal K, Banerjee A, Pal S, et al (2018) Detection, characterization, and antibiogram of extended-spectrum beta-lactamase Escherichia coli isolated from bovine milk samples in West Bengal, India. Vet world 11:1423–1427. https://doi.org/10.14202/VETWORLD.2018.1423-1427
Bevan ER, Jones AM, Hawkey PM (2017) Global epidemiology of CTX-M β-lactamases: Temporal and geographical shifts in genotype. J Antimicrob Chemother 72:2145–2155. https://doi.org/10.1093/jac/dkx146
Carattoli A, Bertini A, Villa L, et al (2005) Identification of plasmids by PCR-based replicon typing. J Microbiol Methods 63:219–228. https://doi.org/10.1016/j.mimet.2005.03.018
Castanheira M, Simner PJ, Bradford PA (2021) Extended-spectrum β -lactamases: an update on their characteristics, epidemiology and detection . JAC-Antimicrobial Resist 3:. https://doi.org/10.1093/jacamr/dlab092
CLSI (2017) Performance standards for antimicrobial susceptibility testing. 27th ed. CLSI supplement M100. Wayne, PA: Clinical and Laboratory Standards Institute
CLSI (2020) Clinical and Laboratory Standards Institute (CLSI). Performance Standards for Antimicrobial Susceptibility Testing. 30th ed. CLSI Suppl M100
Destro, M.T.; Ribeiro VB (2014) Foodborne zoonoses. In: Devine, C., Dikeman M (ed) Encyclopedia of Meat Sciences. Academic Press: Cambridge, MA, USA, pp 17–21
Durmaz R, Otlu B, Koksal F, et al (2009) The optimization of a rapid pulsed-field gel electrophoresis protocol for the typing of Acinetobacter baumannii, Escherichia coli and Klebsiella spp. Jpn J Infect Dis 62
El Garch F, de Jong A, Bertrand X, et al (2018) mcr-1-like detection in commensal Escherichia coli and Salmonella spp. from food-producing animals at slaughter in Europe. Vet Microbiol 213:. https://doi.org/10.1016/j.vetmic.2017.11.014
Ewbank AC, Fuentes-Castillo D, Sacristán C, et al (2022) Extended-spectrum β-lactamase (ESBL)-producing Escherichia coli survey in wild seabirds at a pristine atoll in the southern Atlantic Ocean, Brazil: First report of the O25b-ST131 clone harboring blaCTX-M-8. Sci Total Environ 806:. https://doi.org/10.1016/j.scitotenv.2021.150539
Frank C, Werber D, Cramer JP, et al (2011) Epidemic Profile of Shiga-Toxin–Producing Escherichia coli O104:H4 Outbreak in Germany . N Engl J Med 365:. https://doi.org/10.1056/nejmoa1106483
Frieden T (2013) CDC. Antibiotic Resistance Threats in the United States, 2019. Atlanta, GA: U.S. Department of Health and Human Services, CDC; 2019. Centers Dis. Control Prev.
Govindarajan DK, Viswalingam N, Meganathan Y, Kandaswamy K (2020) Adherence patterns of Escherichia coli in the intestine and its role in pathogenesis. Med. Microecol. 5
Hung WT, Cheng MF, Tseng FC, et al (2019) Bloodstream infection with extended-spectrum beta-lactamase–producing Escherichia coli: The role of virulence genes. J Microbiol Immunol Infect 52:. https://doi.org/10.1016/j.jmii.2019.03.005
Kaper JB, Nataro JP, Mobley HLT (2004) Pathogenic Escherichia coli. Nat Rev Microbiol 2:123–140. https://doi.org/10.1038/NRMICRO818
Kim YJ, Moon JS, Oh DH, et al (2018) Genotypic characterization of ESBL-producing E. coli from imported meat in South Korea. Food Res Int 107:. https://doi.org/10.1016/j.foodres.2017.12.023
Kluytmans JAJW, Overdevest ITMA, Willemsen I, et al (2013) Extended-spectrum β-lactamase-producing escherichia coli from retail chicken meat and humans: Comparison of strains, plasmids, resistance genes, and virulence factors. Clin Infect Dis 56:. https://doi.org/10.1093/cid/cis929
Lavilla S, González-López JJ, Miró E, et al (2008) Dissemination of extended-spectrum β-lactamase-producing bacteria: The food-borne outbreak lesson. J Antimicrob Chemother 61:. https://doi.org/10.1093/jac/dkn093
Ma F, Xu S, Tang Z, et al (2020) Use of antimicrobials in food animals and impact of transmission of antimicrobial resistance on humans. medcentral.net 3:32–38. https://doi.org/10.1016/j.bsheal.2020.09.004
Momtaz H, Safarpoor Dehkordi F, Rahimi E, et al (2013) Incidence of Shiga toxin-producing Escherichia coli serogroups in ruminant’s meat. Meat Sci 95:. https://doi.org/10.1016/j.meatsci.2013.04.051
Nagy B, Szmolka A, Smole Možina S, et al (2015) Virulence and antimicrobial resistance determinants of verotoxigenic Escherichia coli (VTEC) and of multidrug-resistant E. coli from foods of animal origin illegally imported to the EU by flight passengers. Int J Food Microbiol 209:. https://doi.org/10.1016/j.ijfoodmicro.2015.06.026
Neamati F, Firoozeh F, Saffari M, Zibaei M (2015) Virulence genes and antimicrobial resistance pattern in uropathogenic Escherichia coli isolated from hospitalized patients in Kashan, Iran. Jundishapur J Microbiol 8:. https://doi.org/10.5812/jjm.17514
Nelson DW, Moore JE, Rao JR (2019) Antimicrobial resistance (AMR): Significance to food quality and safety. Food Qual. Saf. 3
Ntuli V, Njage PMK, Buys EM (2017) Extended-spectrum β-lactamase, shigatoxin and haemolysis capacity of O157 and non-O157 E. coli serotypes from producer-distributor bulk milk. Int Dairy J 66:. https://doi.org/10.1016/j.idairyj.2016.11.008
Ombarak RA, Hinenoya A, Awasthi SP, et al (2016) Prevalence and pathogenic potential of Escherichia coli isolates from raw milk and raw milk cheese in Egypt. Int J Food Microbiol 221:. https://doi.org/10.1016/j.ijfoodmicro.2016.01.009
Ouchar Mahamat O, Kempf M, Lounnas M, et al (2021) Epidemiology and prevalence of extended-spectrum β-lactamase- and carbapenemase-producing Enterobacteriaceae in humans, animals and the environment in West and Central Africa. Int. J. Antimicrob. Agents 57
Parussolo L, Sfaciotte RAP, Dalmina KA, et al (2019) Detection of virulence genes and antimicrobial resistance profiles of Escherichia coli isolates from raw milk and artisanal cheese in Southern Brazil. Semin Agrar 40:. https://doi.org/10.5433/1679-0359.2019v40n1p163
Pehlivanlar Önen S, Aslantaş Ö, Şebnem Yilmaz E, Kürekci C (2015) Prevalence of β-Lactamase Producing Escherichia coli from Retail Meat in Turkey. J Food Sci 80:. https://doi.org/10.1111/1750-3841.12984
Ranjbar R, Safarpoor Dehkordi F, Sakhaei Shahreza MH, Rahimi E (2018) Prevalence, identification of virulence factors, O-serogroups and antibiotic resistance properties of Shiga-toxin producing Escherichia coli strains isolated from raw milk and traditional dairy products. Antimicrob Resist Infect Control 7:. https://doi.org/10.1186/s13756-018-0345-x
Rawat D, Nair D (2010) Extended-spectrum β-lactamases in Gram Negative Bacteria. J Glob Infect Dis 2:263. https://doi.org/10.4103/0974-777X.68531
Rupp ME, Fey PD (2003) Extended spectrum β-lactamase (ESBL)-producing enterobacteriaceae: Considerations for diagnosis, prevention and drug treatment. Drugs 63:353–365.
Saravanan M, Ramachandran B, Barabadi H (2018) The prevalence and drug resistance pattern of extended spectrum β–lactamases (ESBLs) producing Enterobacteriaceae in Africa. Microb. Pathog. 114
Shaikh S, Fatima J, Shakil S, et al (2015) Antibiotic resistance and extended spectrum beta-lactamases: Types, epidemiology and treatment. Saudi J Biol Sci 22:. https://doi.org/10.1016/j.sjbs.2014.08.002
Tekiner İH, Özpınar H (2016) Occurrence and characteristics of extended spectrum beta-lactamases-producing enterobacteriaceae from foods of animal origin. Brazilian J Microbiol 47:. https://doi.org/10.1016/j.bjm.2015.11.034
Tóth AG, Csabai I, Krikó E, et al (2019) Raw milk for human consumption may carry antimicrobial resistance genes. bioRxiv. https://doi.org/10.1101/853333
Valat C, Haenni M, Saras E, et al (2012) CTX-M-15 extended-spectrum β-lactamase in a shiga toxin-producing Escherichia coli isolate of serotype O111:H8. Appl Environ Microbiol 78:. https://doi.org/10.1128/AEM.06997-11
Wasiński B, Osek J, Różańska H (2014) Antimicrobial resistance of ESBLand AmpC-producing Escherichia coli isolated from meat Antimicrobial resistance of ESBL-and AmpC-producing Escherichia coli isolated from meat. Bull Vet Inst Pulawy 58:567–571. https://doi.org/10.2478/bvip-2014-0088
Younis GA, Elkenany RM, Fouda MA, Mostafa NF (2017) Virulence and extended-spectrum β-lactamase encoding genes in Escherichia coli recovered from chicken meat intended for hospitalized human consumption. Vet World 10:. https://doi.org/10.14202/vetworld.2017.1281-1285
Zurfluh K, Hächler H, Nüesch-Inderbinen M, Stephan R (2013) Characteristics of extended-spectrum β-lactamase- and carbapenemase-producing Enterobacteriaceae isolates from rivers and lakes in Switzerland. Appl Environ Microbiol 79:3021–3026.