Occurrence and Characteristics of Toxigenic Staphylococcus aureus in Retail Foods in Iran

Erfan Ghoreyshizadeh; Meysam Manouchehrifar; Rashid Ramazanzadeh; Hadi Peeri Doghaheh; Mojtaba Amani; Mohsen Arzanlou

doi:10.1089/fpd.2023.0122

Occurrence and Characteristics of Toxigenic Staphylococcus aureus in Retail Foods in Iran

Foodborne Pathog Dis. 2024 Feb 12. doi: 10.1089/fpd.2023.0122. Online ahead of print.

Authors

Erfan Ghoreyshizadeh^{1

2}, Meysam Manouchehrifar³, Rashid Ramazanzadeh¹, Hadi Peeri Doghaheh¹, Mojtaba Amani⁴, Mohsen Arzanlou^{1

2}

Affiliations

¹ Department of Microbiology, School of Medicine, Ardabil University of Medical Sciences, Ardabil, Iran.
² Zoonoses Research Center, Ardabil University of Medical Sciences, Ardabil, Iran.
³ Food Control Laboratory, Deputy of Food and Drug, Ardabil University of Medical Sciences, Ardabil, Iran.
⁴ Department of Medicinal Chemistry, Faculty of Pharmacy, Ardabil University of Medical Sciences, Ardabil, Iran.

PMID: 38346315
DOI: 10.1089/fpd.2023.0122

Abstract

Staphylococcus aureus causes various toxigenic and invasive diseases in humans worldwide. This study examined the prevalence, virulence genes, and antibiotic resistance of S. aureus isolates collected from 894 retail food samples in Ardabil, Iran. Staphylococcal cassette chromosome mec (SCCmec), spa, and multilocus sequence typing methods were employed to further investigate the molecular characteristics of methicillin-resistant S. aureus (MRSA) isolates. The results revealed that 11.18% (n = 100) of food samples exhibited contamination with S. aureus (10.50% methicillin-sensitive S. aureus [MSSA] and 0.67% MRSA). Notably, raw minced meat (29.41%), Faloodeh (25%), and Olivier salad (21.42%) emerged as the most frequently contaminated food items. Among the 100 isolates of S. aureus, 94% were characterized as MSSA, with the remaining 6% identified as MRSA. The highest resistance was observed for penicillin (12%). MRSA isolates exhibited significantly higher resistance rates. Seventy-nine percent of the isolates were positive for sea, 14% for seb, 8% for a sec, and 0% for sed enterotoxin-encoding genes. Sixteen percent of isolates harbored two or more staphylococcal enterotoxin genes, simultaneously. Moreover, 97%, 94%, 24%, and 22% of isolates were positive for hla, hld, tst, and pvl virulence-encoding genes, respectively. No isolate was positive for the exfoliative toxins encoding eta and etb genes. MRSA isolates belonged to CC8 (n = 4) and CC22 (n = 2). Isolates in CC8 belonged to lineage ST239-MRSA-III and spa type t030; the isolates in CC22 belonged to ST22-MRSA-IV and spa types t310 and t223. In conclusion, a relatively high proportion of our retail food samples were contaminated with S. aureus. The high incidence of isolates with toxigenic genes raises serious health concerns. Furthermore, the presence of MRSA lineages linked to humans suggests that retail foods may be contaminated with human origin.

Keywords: methicillin-resistant Staphylococcus aureus; multilocus sequence typing; retail food; spa typing; virulence genes.