Prevalence, antimicrobial resistance, and genotyping of Shiga toxin-producing Escherichia coli in foods of cattle origin, diarrheic cattle, and diarrheic humans in Egypt

Walid Elmonir; Samar Shalaan; Amin Tahoun; Samy F Mahmoud; Etab M Abo Remela; Radwa Eissa; Hanem El-Sharkawy; Mustafa Shukry; Rasha N Zahran

doi:10.1186/s13099-021-00402-y

Prevalence, antimicrobial resistance, and genotyping of Shiga toxin-producing Escherichia coli in foods of cattle origin, diarrheic cattle, and diarrheic humans in Egypt

Gut Pathog. 2021 Feb 5;13(1):8. doi: 10.1186/s13099-021-00402-y.

Authors

Walid Elmonir¹, Samar Shalaan², Amin Tahoun³, Samy F Mahmoud^{4

5}, Etab M Abo Remela^{6

7}, Radwa Eissa⁸, Hanem El-Sharkawy⁹, Mustafa Shukry¹⁰, Rasha N Zahran¹¹

Affiliations

¹ Department of Hygiene and Preventive Medicine (Zoonoses), Faculty of Veterinary Medicine, Kafrelsheikh University, Kafrelsheikh, Egypt. walid.elmonir@gmail.com.
² Department of Hygiene and Preventive Medicine (Zoonoses), Faculty of Veterinary Medicine, Kafrelsheikh University, Kafrelsheikh, Egypt.
³ Department of Animal Medicine, Faculty of Veterinary Medicine, Kafrelsheikh University, Kafrelsheikh, Egypt.
⁴ Department of Biotechnology, College of Science,, Taif University, P.O. Box 11099, Taif, 21944, Saudi Arabia.
⁵ Food Research Institute, Agriculture Research Center, Giza, Egypt.
⁶ Department of Bacteriology, Mycology and Immunology, Faculty of Veterinary Medicine, Kafrelsheikh University, Kafrelsheikh, Egypt.
⁷ Department of Biology, College of Science, Taibah University, Madina, Saudi Arabia.
⁸ Department of Microbiology and Immunology, Faculty of Medicine, Tanta University, Tanta, Egypt.
⁹ Department of Poultry and Rabbit Diseases, Faculty of Veterinary Medicine, Kafrelsheikh University, Kafrelsheikh, Egypt.
¹⁰ Department of Physiology, Faculty of Veterinary Medicine, Kafrelsheikh University, Kafrelsheikh, Egypt.
¹¹ Department of Bacteriology, Mycology, and Immunology, Faculty of Veterinary Medicine, University of Sadat City, Sadat, Egypt.

Abstract

Shiga toxin-producing Escherichia coli (STEC) is a pathotype of E. coli that causes enteric and systemic diseases ranging from diarrhoea to severe hemorrhagic colitis (HC) and hemolytic uremic syndrome (HUS). The emergence of multidrug-resistant (MDR) STEC from cattle sources has increased public health risk and limited treatment options. The prevalence of STEC was investigated in 200 raw food samples (milk and beef samples) and 200 diarrheic samples (cattle and human samples) in a matched region. The presence of stx genes (stx1 and stx2), carbapenemase-encoding genes (bla_VIM, bla_NDM-1, and bla_IMP), and extended-spectrum β-lactamase (ESBL)-encoding genes (bla_TEM group, bla_CTX-M1 group, and bla_OXA-1 group) was screened by polymerase chain reaction (PCR). Antibiogram and Enterobacterial repetitive intergenic consensus (ERIC)-PCR were also conducted. STEC isolates were identified in 6.5% (13/200) of food samples [6% (6/100) of milk and 7% (7/100) of beef samples] and in 11% (22/200) of diarrheic cases [12% (12/100) of cattle and 10% (10/100) of human samples]. We found that O26 (4.5%, 18/400) and O111 (1.5%, 6/400) were the most prevalent STEC serovars and were found more commonly in diarrheic samples. STEC strains with both stx genes, stx2 only, and stx1 only genotypes were present in 62.9% (22/35), 20% (7/35), and 17.1% (6/35) of isolates, respectively. Carbapenemase-producing STEC (CP STEC) isolates were found in 1.8% (7/400) of samples [0.5% (1/200) of foods and 3% (6/200) of diarrheic cases]. The bla_VIM gene was detected in all CP STEC isolates, and one human isolate carried the bla_NDM-1 gene. ESBL-producing STEC strains were detected in 4.3% (17/400) of samples [1.5% (3/200) of food samples and 7% (14/200) of diarrheic cases]. The bla_TEM, bla_CTX-M1, and bla_OXA-1 genes were detected in 42.9% (15/35), 28.6% (10/35), and 2.9% (1/35) of STEC isolates, respectively. Approximately half (51.4%, 18/35) of STEC isolates were MDR STEC; all CP STEC and ESBL-producing STEC were also MDR STEC. The highest antimicrobial resistance rates were found against nalidixic acid (51.4%) and ampicillin (48.6%), whereas the lowest rates were reported against gentamicin (5.7%) and ciprofloxacin (11.4%). MDR STEC strains were 5.3 times more likely to be found in diarrheic cases than in foods (P = 0.009, 95% CI 1.5-18.7). ERIC-PCR was used for genotyping STEC isolates into 27 different ERIC-types (ETs) with a discrimination index of 0.979. Five ETs showed clusters of 2-4 identical isolates that shared the same virulence and antibiotic resistance genetic profile. Human isolates matched food isolates in two of these ET clusters (the O26 CP STEC cluster and the O111 STEC cluster), highlighting the potential cross-species zoonotic transmission of these pathogens and/or their genes in the study region. This is the first detection of CP STEC in milk and diarrheic cattle in Egypt.

Keywords: Carbapenemase genes; Cattle; Extended-spectrum β-lactamase genes; Multidrug-resistant; Public health risk; Shiga toxin-producing Escherichia coli.