Retail Chicken Carcasses as a Reservoir of Multidrug-Resistant Salmonella

Abstract

Salmonella is a major cause of foodborne disease outbreaks worldwide, mainly through poultry. Recently, there has been an increase in multidrug-resistant (MDR) Salmonella infections globally. The increased drug resistance results in increased costs and poorer health outcomes due to unavailability or delayed treatment. This study aims to determine the prevalence of Salmonella in retail raw chicken meat and identify their antimicrobial resistance profiles. A total of 270 retail raw chicken carcasses (local and imported) were collected from three hypermarket chains in Qatar between November 2017 and April 2018. Thirty carcasses were contaminated with Salmonella (11.11%). The prevalence of Salmonella in locally produced chicken was higher than in imported chicken (OR = 2.56, 95% CI: 1.18-5.53, p = 0.016). No significant differences were found between the prevalence and storage temperature or hypermarket chain. The highest resistance rates in the isolates were reported to tetracycline (73.7%) followed by nitrofurantoin (53.3%), ampicillin (50%), amoxicillin-clavulanic acid, ceftriaxone (26.7%), and ciprofloxacin (23.3%). Eight isolates were potential extended-spectrum β-lactamase-producers, all in imported frozen chicken (p < 0.0001). Additionally, 43.3% of the isolates were MDR and associated with frozen chicken (OR = 16.88, 95% CI: 2.55-111.47, p = 0.002). The findings indicate that while the prevalence of Salmonella in retail chicken in Qatar is moderate, a large proportion of them are MDR.

Keywords: AMR; Salmonella; foodborne; retail chicken.

FIG. 1.

Flowchart of the Salmonella isolation and identification process. The flow chart describes the sequential process that was used to determine whether a chicken carcass was contaminated with Salmonella. The red boxes on the right detail the exclusion criteria (i.e., sample is not contaminated by Salmonella) at each step of the process. First, the chicken carcasses were homogenized and mixed with SCB to enrich for Salmonella. Second, 20 μL of the SCB broth-homogenate mixture was streaked on HE agar to select for Salmonella and Shigella. HE agar differentiates between the two species through H₂S production in Salmonella, which results in black colonies. The samples that did not have growth on HE agar or had growth without H₂S production were determined not to be contaminated with Salmonella and excluded from subsequent steps. Third, a urease test was performed on the H₂S-producing isolates. Salmonella is urease negative, as such, the urease positive were excluded from the next steps, and the chicken carcasses they came from were determined not to be contaminated with Salmonella. The last two steps in the process were PCR for the invA gene (A conserved gene in Salmonella) and biochemical identification with the Biomic V3 platform. The process resulted in identifying 30 retail chicken carcasses that were positive for Salmonella. SCB, selenite cystine broth; HE, Hektoen Enteric.

FIG. 2.

The Antibiotic resistance profiles in the Salmonella isolated from retail chicken carcasses in Qatar (n = 30). ^aIsolates were classified as susceptible if they were sensitive (S) or intermediate (I) with in vitro antibiotic susceptibility testing. A binomial test was performed to determine whether the difference in proportions between susceptible and resistant isolates is significant. ns: not significant (p > 0.05), *p ≤ 0.05, **p ≤ 0.01, ****p ≤ 0.0001. AMC, amoxicillin-clavulanic acid; AMP, ampicillin; CHL, chloramphenicol; CIP, ciprofloxacin; CRO, ceftriaxone; CST, colistin; ETP, ertapenem; FEP, Cefepime; FOF, Fosfomycin; MEM, meropenem; NIT, nitrofurantoin; SXT, sulfamethoxazole-trimethoprim; TE, tetracycline; TZP, piperacillin-tazobactam.

FIG. 3.

The distribution of the number of phenotypic resistances to up to 14 antibiotics among the Salmonella isolates (n = 30) from retail chicken carcasses in Qatar. Multidrug resistance is defined as the resistance to ≥3 antibiotic classes.