Methicillin- and Vancomycin-Resistant Staphylococcus aureus From Humans and Ready-To-Eat Meat: Characterization of Antimicrobial Resistance and Biofilm Formation Ability

Abstract

Methicillin-resistant and vancomycin-resistant Staphylococcus aureus (MRSA and VRSA) are zoonotic life-threatening pathogens, and their presence in food raises a public health concern. Yet, scarce data are available regarding MRSA and VRSA in both ready-to-eat (RTE) meat and food handlers. This study was undertaken to determine the frequency, antimicrobial resistance, and biofilm-forming ability of MRSA and VRSA isolated from RTE meat (shawarma and burger) and humans (food handlers, and hospitalized patients) in Zagazig city, Sharkia Governorate, Egypt. We analyzed 176 samples (112 human samples: 72 from hospitalized patients and 40 from food handlers, 64 RTE meat samples: 38 from shawarma and 26 from burger). Using phenotypic, PCR-based identification of nuc gene and matrix-assisted laser desorption ionization-time of flight mass spectrometry (MALDI-TOF MS), 60 coagulase-positive S. aureus (COPS) isolates were identified in the samples as follow: RTE meat (15/64, 23.4%), hospitalized patients (33/72, 45.8%) and food handlers (12/40, 30%). All the COPS isolates were mecA positive (and thus were classified as MRSA) and multidrug resistant with multiple antibiotic resistance indices ranging from 0.25 to 0.92. Overall, resistance to cefepime (96.7%), penicillin (88.3%), were common, followed by ampicillin-sulbactam (65%), ciprofloxacin (55%), nitrofurontoin (51.7%), and gentamicin (43.3%). VRSA was detected in 30.3% of COPS hospitalized patient’s isolates, 26.7% of COPS RTE meat isolates and 25% of COPS food handler’s isolates. VanA, vanB, or both genes were detected in 64.7, 5.9, and 29.4% of all VAN-resistant isolates, respectively. The majority of the COPS isolates (50/60, 83.3%) have biofilm formation ability and harbored icaA (76%), icaD (74%), icaC (50%), and icaB (46%) biofilm-forming genes. The bap gene was not detected in any of the isolates. The ability of MRSA and VRSA isolates to produce biofilms in addition to being resistant to antimicrobials highlight the danger posed by these potentially virulent microorganisms persisting in RTE meat, food handlers, and patients. Taken together, good hygiene practices and antimicrobial surveillance plans should be strictly implemented along the food chain to reduce the risk of colonization and dissemination of MRSA and VRSA biofilm-producing strains.

High levels of biofilm formation and prevalence of biofilm-associated genes in Staphylococcus aureus isolated from food handlers in Brazil

“…Our ndings are compatible with the prior studies that identi ed the icaAD genes are su cient for strong bio lm formation (Arciola et al 2001;Wang et al 2018). However, other authors observed a lower production of icaAD in comparison to the icaADBC expressed simultaneously (Chen et al 2020;Saber et al 2022). This divergence can be explained because of the type of sources that the isolates were obtained from and the exposure to external conditions, such as temperature, pH variation, or other substances that promote the bio lm formation level (Miao et al 2019).…”

“…on several surfaces in kitchen environments, such as knives, sinks, raw meat cutting boards and baking worktops are associated with food handlers carrying S. aureus in cavities nasal and hands (Benjelloun Touimi et al 2020). On the other hand, Staphylococcal bio lm represents one of the greatest risks to food security, since the production of this virulence factor is a risk to the persistence of S. aureus in the kitchen environment, increasing the potential exposure to food and utensils and equipment used (Saber et al 2022).…”

Characterization of the virulence, agr typing and antimicrobial resistance profile of Staphylococcus aureus strains isolated from food handlers in Brazil

“…In this study, it was observed that S. aureus was isolated in half of the samples of nasal cavities and underside of nails from food handlers. According to Castro et al, 15 Ahmed, 25 and Saber et al 26 the presence of S. aureus in the hands and/or noses of food handlers was of 30%, 25%, and 30%, respectively.…”

Development of a Multiplex Polymerase Chain Reaction-Based DNA Lateral Flow Assay as a Point-of-Care Diagnostic for Fast and Simultaneous Detection of MRSA and Vancomycin Resistance in Bacteremia

“…Primer pairs were designed to allow partial amplification of conserved regions in nuc , mec A, and vancomycin-resistance gene variants A and B ( van A/B). The nuc gene encodes for a thermonuclease specific for S. aureus [ 21 ]; mec A encodes for penicillin-binding protein 2 that is responsible for methicillin resistance [ 22 ], and van A/B encodes for vancomycin-resistance determinants type A and B [ 23 ]. Different sequences of the target genes were downloaded from the National Center for Biotechnology Information (NCBI); the list of accession numbers of the used sequences is provided in Table S1 .…”