Abstract

Simple SummaryCampylobacter species are among the major causes of bacterial foodborne infections. Here, we investigate, for the first time, class 1 integrons and associated gene cassettes among pan drug-resistant (PDR), extensively drug-resistant (XDR), and multidrug-resistant (MDR) Campylobacter species isolated from livestock animals and humans in Egypt. Our results revealed alarming PDR (2.55%) and inordinate XDR (68.94%) and MDR (28.5%) Campylobacter isolates. None of the examined isolates were pan-susceptible. The existence of a novel gene cassette array, namely aacC5-aadA7Δ4 and a putative phage tail tape measure protein on class 1 integrons of Campylobacter species is the most highlighted novelty of the current study. Evidence from this study showed the possibility of Campylobacter–bacteriophage interactions as well as treatment failure in animals and humans due to horizontal gene transfer mediated by class 1 integrons.Campylobacter species are common commensals in the gastrointestinal tract of livestock animals; thus, animal-to-human transmission occurs frequently. We investigated for the first time, class 1 integrons and associated gene cassettes among pan drug-resistant (PDR), extensively drug-resistant (XDR), and multidrug-resistant (MDR) Campylobacter species isolated from livestock animals and humans in Egypt. Campylobacter species were detected in 58.11% of the analyzed chicken samples represented as 67.53% Campylobacter jejuni (C. jejuni) and 32.47% Campylobacter coli (C. coli). C. jejuni isolates were reported in 51.42%, 74.28%, and 66.67% of examined minced meat, raw milk, and human stool samples, respectively. Variable antimicrobial resistance phenotypes; PDR (2.55%), XDR (68.94%), and MDR (28.5%) campylobacters were reported. Molecular analysis revealed that 97.36% of examined campylobacters were integrase gene-positive; all harbored the class 1 integrons, except one possessed an empty integron structure. DNA sequence analysis revealed the predominance of aadA (81.08%) and dfrA (67.56%) alleles accounting for resistance to aminoglycosides and trimethoprim, respectively. This is the first report of aacC5-aadA7Δ4 gene cassette array and a putative phage tail tape measure protein on class 1 integrons of Campylobacter isolates. Evidence from this study showed the possibility of Campylobacter–bacteriophage interactions and treatment failure in animals and humans due to horizontal gene transfer mediated by class 1 integrons.

Highlights

  • Thermophilic Campylobacter species, Campylobacter jejuni (C. jejuni) and Campylobacter coli (C. coli) pose veterinary and public health concerns due to their zoonotic potential, the enormous range of reservoir hosts, and persistence in the environment [1]

  • Out of 265 samples of chicken origin, 154 (58.11%) Campylobacter isolates were detected, represented as 67.53% C. jejuni and 32.47% C. coli

  • The higher prevalence of C. jejuni was detected in chicken organs (61.54%), followed by cloacal swabs (57.14%) and chicken muscles (48.00%), while the isolation rate of C. coli from these sources was close to 30%, each

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Summary

Introduction

Thermophilic Campylobacter species, Campylobacter jejuni (C. jejuni) and Campylobacter coli (C. coli) pose veterinary and public health concerns due to their zoonotic potential, the enormous range of reservoir hosts, and persistence in the environment [1]. Most Campylobacter infections are self-limiting and require no therapeutic intervention other than supportive and rehydration therapy. Prompt antimicrobial treatment is employed in immunocompromised individuals, patients whose symptoms are severe or persistent, intense or prolonged enteritis, cases of bacteremia, and those with extraintestinal infections [4]. Attention to the resistance of campylobacters has been launched due to the indiscriminate abuse of antibiotics [5]. Veterinary, and environmental surveys have shown that bacteria harboring integrons are frequently associated with the multidrug-resistant (MDR) phenotype [6]. The extensively drug-resistant (XDR) and pan drug-resistant (PDR) bacteria are epidemiologically significant due to their resistance to multiple antimicrobial agents and to their ominous prospect of being resistant to almost all or all approved antimicrobial agents [7,8]

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