Potential of Natural Phenolic Compounds as Antimicrobial Agents against Multidrug-Resistant Staphylococcus aureus in Chicken Meat

Abstract

Staphylococcus aureus is one of the most widespread foodborne bacteria that cause high morbidity, mortality, and economic loss, primarily if foodborne diseases are caused by pathogenic and multidrug-resistant (MDR) strains. This study aimed to determine the prevalence of S. aureus in chicken meat in Egyptian markets. Thus, this study might be the first to assess the efficiency of different natural phenolic compounds as novel antibacterial agents against MDR S. aureus pathogens isolated from raw chicken meat in the Egyptian market. The incidence and quantification of pathogenic S. aureus were detected in retail raw chicken meat parts (breast, thigh, fillet, and giblets). In total, 73 out of 80 (91.3%) of the chicken meat parts were contaminated, with S. aureus as the only species isolated. Of the 192 identified S. aureus isolates, 143 were coagulase-positive S. aureus and 117 isolates were MDR (81.8%, 117/143). Twenty-two antibiotic resistance profile patterns were detected. One strain was randomly selected from each pattern to further analyze virulence and resistance genes. Extracted DNA was assessed for the presence of antibiotic-resistance genes, i.e., vancomycin-resistance (vanA), aminoglycosides-resistance (aacA-aphD), apramycin-resistance (apmA), and methicillin-resistance (mecA), penicillin-resistance (blaZ), and virulence genes staphylococcal enterotoxins (sea and seb), Panton-Valentine leucocidin (pvl), clumping factor A (clfA), and toxic shock syndrome toxin (tst). Clustering analyses revealed that six S. aureus strains harbored the most virulence and resistance genes. The activity of hydroquinone was significantly higher than thymol, carvacrol, eugenol, and protocatechuic acid. Therefore, phenolic compounds, particularly hydroquinone, could potentially alternate with conventional antibiotics against the pathogenic MDR S. aureus inhabiting raw chicken meat. Hence, this study indicates that urgent interventions are necessary to improve hygiene for safer meat in Egyptian markets. Moreover, hydroquinone could be a natural phenolic compound for inhibiting foodborne pathogens.

Keywords: Staphylococcus aureus; antimicrobials; chicken meat; foodborne pathogen; multidrug resistance; phenolic compounds.

Figure 1

The incidence of S. aureus in different chicken meat samples and the statistical analysis using a t-test showing the significant variation in the contamination between the tested retail raw chicken meat samples.

Figure 2

Clustering analysis showing the incidence of resistance and virulence genes in tested MDR S. aureus strains isolated from different chicken meat samples. mecA–methicillin-resistance, blaZ–penicillin-resistance, vanA–vancomycin-resistance, apmA–apramycin-resistance, aacA–aphD–aminoglycosides-resistance, sea and seb–virulence genes staphylococcal enterotoxins, pvl–Panton–Valentine leucocidin, clfA–clumping factor A, and tst–toxic shock syndrome toxin.

Figure 3

Neighbor-joining tree based on 16S rRNA gene sequences showing the phylogenetic position of the selected resistance and virulence genes producing MDR S. aureus strains within closely related taxa. The numbers on tree branches indicate the percentages of bootstrap sampling (≥50%) derived from 1000 replicates. The scale bars indicate substitutions per nucleotide position.

Figure 4

Scanning electron microscope photomicrographs of S. aureus before (A) and after the treatment with hydroquinone (B).

Figure 5

The experimental setup procedures to identify, quantify, and characterize biofilm-producing S. aureus from raw chicken meat samples and investigate the activity of various phenolic compounds against the selected S. aureus strains.

Figure 6

Chemical structures of the phenolic compounds evaluated in this study (A) and the proposed antimicrobial activity of hydroquinone against MDR bacteria (B).