Salmonella enterica is one of the most ubiquitous enteropathogenic bacterial species on earth, and comprises more than 2500 serovars. Widely known for causing non-typhoidal foodborne infections (95%), and enteric (typhoid) fever in humans, Salmonella colonizes almost all warm- and cold-blooded animals, in addition to its extra-animal environmental strongholds. The last few decades have witnessed the emergence of highly virulent and antibiotic-resistant Salmonella, causing greater morbidity and mortality in humans. The emergence of several Salmonella serotypes resistant to multiple antibiotics in food animals underscores a significant food safety hazard. In this review, we discuss the various antibiotic-resistant Salmonella serotypes in food animals and the food supply, factors that contributed to their emergence, their antibiotic resistance mechanisms, the public health implications of their spread through the food supply, and the potential antibiotic alternatives for controlling them.

We investigated the effects of a probiotic bacterium, Propionibacterium freudenreichii, on Salmonella multiplication, motility, and association to and invasion of avian epithelial cells in vitro. Two subspecies of P. freudenreichii (P. freudenreichii subsp. freudenreichii and P. freudenreichii subsp. shermanii) were tested against 3 Salmonella serotypes in poultry, namely, S. Enteritidis, S. Typhimurium, and S. Heidelberg, using co-culture-, motility, multiplication, cell association, and invasion assays. Both strains of P. freudenreichii were effective in reducing or inhibiting multiplication of all 3 Salmonella serotypes in co-culture and turkey cecal contents (P ≤ 0.05). P. freudenreichii significantly reduced Salmonella motility (P ≤ 0.05). Cell culture studies revealed that P. freudenreichii associated with the avian epithelial cells effectively and reduced S. Enteritidis, S. Heidelberg, and S. Typhimurium cell association in the range of 1.0 to 1.6 log10 CFU/mL, and invasion in the range of 1.3 to 1.5 log10 CFU/mL (P ≤ 0.05), respectively. Our current in vitro results indicate the potential of P. freudenreichii against Salmonella in poultry. Follow-up in vivo studies are underway to evaluate this possibility.

Salmonella attached to the poultry skin is a major source of carcass contamination during processing. Once attached to the poultry skin, it is difficult to detach and inactivate Salmonella by commonly used antimicrobial agents since the pathogen is entrapped deeply in the feather follicles and the crevices on the skin. Essential oils could be natural, safe, and effective alternatives to synthetic antimicrobial agents during commercial and organic processing setup. The present study evaluated the efficacy of pimenta (Pimenta officinalis Lindl.) leaf essential oil (PEO), and its nanoemulsion in reducing Salmonella Heidelberg attachment on to turkey (Meleagris gallopavo) skin during simulated scalding (65°C) and chilling (4°C) steps in poultry processing. A multidrug resistant S. Heidelberg isolate from the 2011 ground turkey outbreak in the United States was used in the study. Results showed that PEO and the nanoemulsion resulted in significant reduction of S. Heidelberg attachment on turkey skin. Turkey skin samples treated with 1.0% PEO for 5 min resulted in >2 log10 CFU/sq. inch reduction of S. Heidelberg at 65 and 4°C, respectively (n = 6; P < 0.05). Similarly, skin samples treated with 1.0% pimenta nanoemulsion (PNE) for 5 min resulted in 1.5- and 1.8- log10 CFU/sq. inch reduction of S. Heidelberg at 65 and 4°C, respectively (n = 6; P < 0.05). In addition, PEO and PNE were effective in reducing S. Heidelberg on skin during short-term storage at 4 and 10°C (temperature abuse) (n = 6; P < 0.05). No Salmonella was detected in the dipping solution containing 0.5 or 1.0% PEO or PNE, whereas a substantial population of the pathogen survived in the control dipping solution. The results were validated using scanning electron -, and confocal - microscopy techniques. PEO or PNE could be utilized as an effective antimicrobial agent to reduce S. Heidelberg attachment to turkey skin during poultry processing.

Salmonella Heidelberg ( S. Heidelberg) is a major pathogen implicated in foodborne outbreaks for which poultry products can serve as an epidemiological source. This study determined the efficacy of GRAS-status lemongrass essential oil ( LGEO ) against S. Heidelberg in vitro and on the pathogen's attachment to skin and meat. At first, employing in vitro assays, the effect of LGEO on multidrug-resistant S. Heidelberg multiplication and motility was examined. Biofilm inhibition and inactivation assays were also performed. The quorum-sensing modulating effect of LGEO was determined . In follow-up experiments, chicken skin or meat samples inoculated with S. Heidelberg were treated with various concentrations of LGEO at different time points at simulated scalding (54°C) and chilling (4°C) temperatures. The samples were incubated, and the surviving populations of S. Heidelberg were enumerated to determine if LGEO could be a potential processing aid in poultry operations. Duplicate samples were included in each treatment, and the experiments were repeated at least 3 times. Significant reductions of S. Heidelberg of at least 4.0 log 10 CFU/mL after 24 h in nutrient broth and poultry cecal contents was observed with 0.5% LGEO. Complete inhibition of motility, biofilm formation, and inactivation of pre-formed biofilms was observed with 0.15% LGEO ( P ≤ 0.05). Concentrations of LGEO at 0.5% and 1% affected violacein production ( P ≤ 0.05). On skin samples, all concentrations significantly reduced S. Heidelberg by 1.2 to 3.9 log 10 CFU/sample after 2 min at 54°C. We obtained a significant reduction of the pathogen in meat samples at 54°C and skin samples at 4°C with 2% LGEO. All concentrations significantly reduced S. Heidelberg from the treatment water kept at 4°C and 54°C ( P ≤ 0.05). In conclusion, LGEO could potentially serve as a natural antimicrobial strategy in scalding and chilling waters to reduce S. Heidelberg during processing. However, additional studies are warranted before recommending its commercial use.

The foodborne illnesses associated with poultry meat due to Salmonella are a major concern in the United States. In this study, the antimicrobial efficacy of carvacrol, eugenol, thyme essential oil, and trans-cinnamaldehyde was determined against different Salmonella serotypes in vitro and on turkey breast cutlets. Minimum inhibitory concentration (MIC) and minimum bactericidal concentration (MBC) of antimicrobial agents were determined using a microdilution colorimetric assay. Carvacrol was the most effective antimicrobial agent since it exhibited the lowest MIC and MBC (0.313 μL/mL, respectively) in culture media against Salmonella. Turkey breast cutlets inoculated with Salmonella Enteritidis, Salmonella Heidelberg, and Salmonella Typhimurium were dip treated with different concentrations (0.5, 1, 2, and 5% vol/vol) of carvacrol, eugenol, thyme essential oil, and trans-cinnamaldehyde for 2 min. Samples were analyzed after 24-h storage at 4°C for recovery of Salmonella. Significant reductions of Salmonella (p≤0.05) on turkey breast cutlets were obtained with 1, 2, and 5% treatments. These compounds exhibited a concentration-dependent response on turkey breast cutlets against Salmonella. For example, 1% carvacrol resulted in 1.0 log colony-forming units (CFU)/g reduction of Salmonella whereas 5% carvacrol caused 2.6 log CFU/g reduction. Based on its efficacy in the 2-min dip study, carvacrol was selected for 30-s and 60-s dip treatments of Salmonella-inoculated turkey breast cutlets. Dipping turkey breast cutlets in 5% carvacrol for 30 s and 60 s resulted in 1.0 and 1.8 log reductions of Salmonella (p≤0.05), respectively. None of the antimicrobial agents caused any changes in the meat pH (p>0.05). In conclusion, this study revealed that plant-derived compounds such as carvacrol can reduce Salmonella on turkey breast cutlets without changing the pH of meat.