Abstract
The emergence of extensive drug-resistant (XDR) Salmonella in livestock animals especially in poultry represents a serious public health and therapeutic challenge. Despite the wealth of information available on Salmonella resistance to various antimicrobials, there have been limited data on the genetic determinants of XDR Salmonella exhibiting co-resistance to ciprofloxacin (CIP) and tigecycline (TIG). This study aimed to determine the prevalence and serotype diversity of XDR Salmonella in poultry flocks and contact workers and to elucidate the genetic determinants involved in the co-resistance to CIP and TIG. Herein, 115 Salmonella enterica isolates of 35 serotypes were identified from sampled poultry (100/1210, 8.26%) and humans (15/375, 4.00%), with the most frequent serotype being Salmonella Typhimurium (26.96%). Twenty-nine (25.22%) Salmonella enterica isolates exhibited XDR patterns; 25 out of them (86.21%) showed CIP/TIG co-resistance. Exposure of CIP- and TIG-resistant isolates to the carbonyl cyanide 3-chlorophenylhydrazone (CCCP) efflux pump inhibitor resulted in an obvious reduction in their minimum inhibitory concentrations (MICs) values and restored the susceptibility to CIP and TIG in 17.24% (5/29) and 92% (23/25) of the isolates, respectively. Molecular analysis revealed that 89.66% of the isolates contained two to six plasmid-mediated quinolone resistance genes with the predominance of qepA gene (89.66%). Mutations in the gyrA gene were detected at codon S83 (34.62%) or D87 (30.77%) or both (34.62%) in 89.66% of XDR Salmonella. The tet(A) and tet(X4) genes were detected in 100% and 3.45% of the XDR isolates, respectively. Twelve TIG-resistant XDR Salmonella had point mutations at codons 120, 121, and 181 in the tet(A) interdomain loop region. All CIP and TIG co-resistant XDR Salmonella overexpressed ramA gene; 17 (68%) out of them harbored 4-bp deletion in the ramR binding region (T-288/A-285). However, four CIP/TIG co-resistant isolates overexpressed the oqxB gene. In conclusion, the emergence of XDR S. enterica exhibiting CIP/TIG co-resistance in poultry and humans with no previous exposure to TIG warrants an urgent need to reduce the unnecessary antimicrobial use in poultry farms in Egypt.
Highlights
Salmonella enterica subspecies enterica serovars are the leading cause of food-borne zoonoses worldwide, accounting for 93.8 million cases of gastroenteritis and 155000 deaths annually (Majowicz et al, 2010)
Statistical analysis revealed that the difference in the infection rates of all birds with Salmonella species was significant (p-value = 0.04), whereas it was nonsignificant among each poultry species (p-value > 0.05)
Biochemical reactions for presumptive identification of Salmonella isolates indicated that all tested isolates were positive for methyl red, Simmons’ citrate, and oxidase tests and displayed characteristic reactions on triple sugar iron and lysine decarboxylase agar media, whereas the analyzed isolates were negative for indole and Voges–Proskauer tests
Summary
Salmonella enterica subspecies enterica serovars are the leading cause of food-borne zoonoses worldwide, accounting for 93.8 million cases of gastroenteritis and 155000 deaths annually (Majowicz et al, 2010). Multiple S. enterica serovars originating from poultry have been considered the potential source of human salmonellosis through the consumption of contaminated bird meat (Hoelzer et al, 2011; Thomas et al, 2017; Anbazhagan et al, 2019). More alarming than the MDR is the recent emergence of the extensive drug-resistant [XDR, i.e., resistant to one or more agents in all antimicrobial categories except two or fewer from the worksheet for defining and categorizing the isolates according to Magiorakos et al (2012)] Salmonella such as the previously reported Salmonella Indiana (Wang et al, 2017) and Salmonella Typhi (Klemm et al, 2018; Saeed et al, 2019). It is worthy to note that the available studies on the mechanisms of antimicrobial resistance in S. enterica and in particular the XDR isolates have focused on the resistance to a single antibiotic (Chen et al, 2017; Zhang et al, 2017) without deciphering the molecular rationale behind the emergence of cross-antibiotic resistance, including to unrelated drugs
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