Antibiotic Resistance, Biofilm Formation, and Molecular Epidemiology of Foodborne Staphylococcus aureus Isolated in Northwest Hubei Province, China

Abstract

Staphylococcus aureus is a common pathogen responsible for foodborne infections worldwide. This study investigated the antibiotic resistance profiles, biofilm formation capacity, and molecular epidemiological characteristics of foodborne S. aureus isolates from northwest Hubei Province, China, as well as the correlation among these factors. Among the 303 food samples collected from Xiangyang, Suizhou, and Shiyan cities, 41 yielded non-duplicate S. aureus strains. Of the 41 S. aureus isolates, 8 (19.51%) were identified as MRSA, while 33 (80.49%) were methicillin-susceptible S. aureus (MSSA). High resistance was observed to penicillin (78.05%), tetracycline (43.90%), and erythromycin (31.71%), with MRSA strains demonstrating significantly stronger resistance profiles than MSSA strains. Among MRSA isolates, 50% (4/8) demonstrated strong biofilm-forming capacity, compared to only 9.09% (3/33) of MSSA isolates. Strong biofilm formation was observed more frequently in isolates from frozen meat (66.67%, 4/6) than in those from vegetarian salads (0%, 0/9) or fresh meat (12.50%, 2/16). The prevalence of Panton-Valentine leukocidin (PVL) gene was higher in MRSA strains, whereas enterotoxin genes were more commonly found in MSSA strains, though differences between groups were not statistically significant. The primary epidemic clones identified were CC88-ST88-t1376/t437, CC7-ST7-t091/t3884, and CC5-ST6/ST462-t701/t165, constituting 63.41% (26/41) of isolates. The CC59-ST59/338 strain exhibited a pronounced capacity for strong biofilm formation. SCCmecII-CC15-ST15-t085 and SCCmecIII-CC7-ST7-t3884 strains exhibited the highest antibiotic resistance, with resistance to 9 and 7 antibiotics, whereas CC88-ST88-t1376, CC7-ST7-t091, and CC5-ST6-t701 showed resistance to fewer than three antibiotics. The findings enhance the understanding of the drug resistance profiles and molecular epidemiology of foodborne S. aureus, providing a foundation for more effective control measures.

Keywords: Staphylococcus aureus; antimicrobial susceptibility; biofilm; foodborne; multilocus sequence typing; virulence genes.

FIGURE 1

Heatmap of antimicrobial resistance patterns in MRSA and MSSA isolates. The heatmap was generated using R version 4.0.3. X‐axis: Tested antimicrobial agents; Y‐axis: Bacterial isolates grouped by strain type (MRSA/MSSA). Resistance color‐coding: Susceptible (blue), intermediate (white), resistant (red).

FIGURE 2

Prevalence of MRSA and MSSA isolates across food categories in Northwest Hubei Province, China. Food sources: Fresh meat (Fre, n = 16), frozen meat (Fro, n = 6), cooked meat products (Coo, n = 4), vegetarian salads (VS, n = 9), bean products (Bp, n = 4), rice and noodle products (Rnp, n = 2). Bars represent detection rates (%) of methicillin‐resistant (MRSA) and methicillin‐susceptible (MSSA) Staphylococcus aureus strains (total isolates: N = 41).

FIGURE 3

Comparative prevalence of biofilm‐associated genes in food‐derived MRSA versus MSSA isolates from Northwest Hubei, China. Bar chart showing PCR‐based detection rates (%) of adhesion genes: icaAD, icaBC, SasG, SasC, fnbpA, and pls. Columns represent methicillin‐resistant (MRSA, n = 8) and methicillin‐susceptible (MSSA, n = 33) Staphylococcus aureus strains.

FIGURE 4

Molecular characterization of food‐derived Staphylococcus aureus isolates (n = 41) from northwest Hubei, China. MLST, multilocus sequence typing; SCCmec, Staphylococcal Cassette Chromosome mec; spa, staphylococcal protein A; ST, sequence type.

FIGURE 5

Minimum‐spanning tree constructed with PHYLOViZ online depicting genetic relationships among 41 foodborne Staphylococcus aureus strains isolated from northwest Hubei Province, China. Each node represents a unique ST type. The size of each node corresponds to the number of strains. The length between two nodes reflects the genetic distance between the two bounding ST types. The color partition of each disc corresponds to the proportion of the SPA types. Figures on the nodes are ST numbers.