Prevalence, characterization and antimicrobial susceptibility patterns of extraintestinal pathogenic Escherichia coli from chicken carcasses in Gauteng Province, South Africa

Abstract

Extraintestinal pathogenic Escherichia coli (ExPEC) strains are adaptable bacteria often associated with urinary tract, kidney, bloodstream and other extraintestinal infections. Extraintestinal pathogenic Escherichia coli infections pose a global public health threat due to their economic impact and management challenges, with poultry meat and other meat products implicated in the spread of the disease. However, in South Africa, there is scarcity of published data on the contamination level and role that poultry meat plays in transmitting ExPEC. The purpose of the study was to determine the prevalence, genetic characteristics and antimicrobial susceptibility profile of ExPEC from chicken carcasses sampled from the Gauteng Province. The study utilized a stratified proportional sampling method to analyse 404 chicken carcasses collected from four abattoirs across five municipalities in Gauteng Province. An additional 63 historically persevered freeze-dried isolates from poultry were included to strengthen this study. Most Probable Number method was used for detection of Escherichia coli. Antimicrobial susceptibility testing was conducted using the minimum inhibition concentration method against 12 antibiotics. Selected classes of antibiotics include cephalosporin, macrolide, phenicol, tetracycline, penicillin, fluoroquinolone, aminoglycoside, and sulphonamide. This selection is motivated by the necessity to comprehend, monitor, and address the emergence of resistance in a common Gram-negative bacteria including ExPEC. Conventional polymerase chain reaction was used to confirm ExPEC presence, alongside gene characterization through virulence genotyping, phylogenetic grouping, phenotypic resistance, and pathotyping. The overall prevalence of E. coli was 93% with 4% confirmed as ExPEC. The ExPEC isolates predominantly carried multiple virulence genes: ompA (100%), mat (83%), kpsm (65%), both csg and sitA with (57%), sat and traT (52%) virulent genes. The highest antibiotic-resistant rates were observed in tetracycline-32-4mg/L (57%), ciprofloxacin- 32-4mg/L (43%), and gentamicin-16-0.25mg/L (39%). However, ceftriaxone, ceftiofur, and cefoxitin (9%) exhibited the lowest antibiotic resistance. The genes associated with the highest phenotypic resistance were sul3 (43%) and tetA (39%). The phylogenetic groups indicated that majority of the ExPEC isolates belonged to group A (39%), group B2 (35%) lastly both groups B1 and D (13%). Class 3 integron was detected in 74% isolates followed by Class 1 integron (35%) and Class 2 (9%). The NMEC pathotype was rare among these isolates, while 13% and 26% distribution were observed in APEC, UPEC, and SEPEC pathotypes. In conclusion, it is evident that while ExPEC occurrence is rare, E. coli is consistently isolated from chicken meat. Despite its low frequency, ExPEC demonstrated a high prevalence of Class 3 integron and virulence-encoding genes that are crucial for colonization and survival. These factors contribute to the spread of resistance genes and emergence of multidrug resistance. Future research should utilize whole genome sequencing for comprehensive molecular characterization, focusing on plasmids and serotyping to differentiate strains from formal and informal abattoirs, which may reveal sources of contamination.