Virulence profile and genetic variability of Staphylococcus aureus isolated from artisanal cheese

Abstract

The objectives of this study were to characterize Staphylococcus aureus isolated from artisanal and industrialized Minas frescal cheeses, to determine their antimicrobial susceptibility profile as well as the genetic similarity among the isolates. The isolates were also tested for staphylococcal enterotoxin genes and other virulence factors. Fifty-six artisanal raw milk cheeses sold at street fairs and 10 industrialized cheeses commercialized in supermarkets of Goiânia, Goiás, were analyzed. Staphylococcus aureus was confirmed in 19 samples (33.9%) of artisanal cheese by detection of femA gene, in which 29 isolates were obtained. These isolates were submitted to the antimicrobial susceptibility test and classified into 9 different profiles (A-I). Thirteen isolates (44.8) were resistant to penicillin and 3 (10.3) to tetracycline, with 2 (7.4) resistant to both. The multiplex PCR technique was performed to detect virulence genes that code for the production of hemolysins (Hla and Hlb), toxic shock syndrome toxin (TSST-1), exfoliative toxins (ETa and ETb), and staphylococcal enterotoxins [SE; SEA-SEE, SEG-SEJ, SEM-SEO]. All the isolates amplified for the hla gene and 14 (48.3%) for the hlb gene. The seh gene was the most frequently detected (n=11, 37.9%), followed by seo gene (n=3; 10.3%). In one isolate (3.4%), 4 enterotoxins genes were detected, and in another, 6 (3.4%) were detected. The comparison performed by pulsed-field gel electrophoresis of the 29 isolates revealed 18 genotypic profiles, which were grouped into 5 clusters. The genotyping found high genetic similarity among the isolates. Identical isolates were obtained from different samples and one sample showed more than one genetically different isolate. The high prevalence of S. aureus in the Minas Frescal cheese samples, as well as the detection of toxin encoding genes identified in this study, warns of the necessity to reduce the contamination levels in this type of cheese through monitoring and controlling the production and trade of the product.

Investigation of mecA gene, virulence traits and antibiotic resistance profiles in methicillin‐resistant Staphylococcus aureus isolates from dairy products

“…In the present survey, tss , eta , etb , and pvl genes were not found in the MRSA and methicillin‐susceptible S. aureus strains. Our findings are consistent with the results of Ferreira et al () and Song et al () which documented the absence of these genes in MRSA strains isolated from cheese and milk samples, respectively. A similar observation was made in the study conducted in Turkey of Sudagidan and Aydin () who did not detect eta , etb , and tst genes in food isolates of methicillin‐susceptible S. aureus .…”

“…The same result was found by Ektik et al (), and similar results were published by Papadopoulos et al () with 99.3% resistance and by Can et al () with 95% resistance. Consistent with our data, several studies performed in different countries also reported resistance to tetracycline (Can & Çelik, ; Ferreira et al, ; Oniciuc et al, ; Pamuk et al, ; Papadopoulos et al, ; Traversa et al, ), clindamycin (Can & Çelik, ; Pamuk et al, ; Traversa et al, ), and chloramphenicol (Pamuk et al, ; Papadopoulos et al, ). In addition to antibiotics tested in the present study, resistance to erythromycin (Can & Çelik, ; Pamuk et al, ; Traversa et al, ), ampicillin (Can & Çelik, ; Ektik et al, ), and ciprofloxacin (Oniciuc et al, ; Papadopoulos et al, ) has been reported in milk and dairy isolates of MRSA.…”

“…Fourteen of butter samples harbored MRSA. In 20, 22, 138, 149, 178, 216, 278, 404, 465, 504, 598, and 636 2012; Ferreira et al, 2016;Oniciuc et al, 2015;Pamuk et al, 2012;Papadopoulos et al, 2018;Traversa et al, 2015), clindamycin (Can & Çelik, 2012;Pamuk et al, 2012;Traversa et al, 2015), and chloramphenicol (Pamuk et al, 2012;Papadopoulos et al, 2018). In addition to antibiotics tested in the present study, resistance to erythromycin (Can & Çelik, 2012;Pamuk et al, 2012;Traversa et al, 2015), ampicillin (Can & Çelik, 2012;Ektik et al, 2017), and ciprofloxacin (Oniciuc et al, 2015;Papadopoulos et al, 2018) has been reported in milk and dairy isolates of MRSA.…”

“…Staphylococcal toxic shock syndrome toxin (TSST‐1) is a member of the pyrogenic toxin super‐antigen family and is produced by foodborne S. aureus . This toxin generates an immune hyper‐response in the host (Ferreira et al, ). The virulence trait of exfoliative toxins is responsible for the loss of keratinocytes and cell–cell adhesion, inducing peeling of the skin and blister formation and is secreted by certain S. aureus strains.…”

“…Staphylococcal toxic shock syndrome toxin (TSST-1) is a member of the pyrogenic toxin super-antigen family and is produced by foodborne S. aureus. This toxin generates an immune hyper-response in the host (Ferreira et al, 2016).…”