Emergence of methicillin-resistant Staphylococcus aureus (MRSA) ST8 in raw milk and traditional dairy products in the Tizi Ouzou area of Algeria

Abstract

Staphylococcus aureus is one of the leading causes of food-borne illness worldwide. Raw milk and dairy products are often contaminated with enterotoxigenic strains of this bacterium. Some of these strains carry antimicrobial resistance, leading to a potential risk for consumers. The aim of this study was to characterize S. aureus strains circulating in raw milk and traditional dairy products for carriage of staphylococcal enterotoxin (se) genes and antimicrobial resistance. Overall, 62 out of 270 samples (23%) were contaminated with S. aureus, and 69 S. aureus strains were identified. We studied the enterotoxin genes using 2 multiplex PCR targeting 11 se genes. Seventeen (24.6%) isolates carried one or more genes encoding for staphylococcal enterotoxins. The most commonly detected se genes were seb and sep, followed by seh, sea, and see. Using the disk diffusion method, we found that resistance to penicillin G and tetracycline was the most common. Eleven isolates of methicillin-resistant S. aureus (MRSA) carried the mecA gene. All MRSA isolates belonged to the same spa type (t024) and sequence type (ST8), and carried the seb and sep enterotoxin genes. However, none of them carried the Panton Valentine leukocidin gene (lukF/S-PV). The presence of enterotoxigenic S. aureus strains, including MRSA, in raw milk and dairy products, raises a serious public health concern, because these strains may cause food poisoning outbreaks, be disseminated to the population, or both.

Enterotoxin genes and antimicrobial resistance in Staphylococcus aureus isolated from food products in Algeria

“…The antimicrobial susceptibility of MRSA strains revealed that all of these strains were resistant to antimicrobial agent other than b-lactams, such as tetracycline, aminoglycosides (tobramycin and neomycin), macrolides (erythromycin) and chloramphenicol, indicating a multidrug-resistant phenotype, as in other studies (Caruso et al 2016;Parisi et al 2016;Chaalal et al 2018;Titouche et al 2019;Papadopoulos et al 2019b). None of our MRSA strains carried the genes encoding the Panton Valentine leucocidin (lukF/S-PV), although these genes have been detected by others in raw milk samples (Haran et al 2012;Basanisi et al 2017;Chaalal et al 2018), meat (Hanson et al 2011;Thapaliya et al 2017; Chaalal et al 2018) and ready to eat foods (Chaalal et al 2018;Islam et al 2019).…”

“…Chaalal et al (2018) reported a rate of 21Á5% in various type of foods, including raw milk, meat and pastry. A low prevalences were observed in other studies conducted in Algeria, with a values of 4Á1% in raw milk and traditional dairy products (Titouche et al 2019) and 13Á6% (Mairi et al 2019). All MRSA strains of our study were isolated from raw milk and dairy products (rayeb).…”

“…All MRSA strains of our study were isolated from raw milk and dairy products (rayeb). As reported by many authors, raw milk has been identified as a source of MRSA demonstrating the potential food safety of contaminated milk and dairy products entering the human food chain (Carfora et al 2015;Caruso et al 2016;Parisi et al 2016;Basanisi et al 2017;Giaciniti et al 2017;Papadopoulos et al 2019b;Titouche et al 2019). However, MRSA was also isolated in meat (De Boer et al 2009;Hanson et al 2011;Thapaliya et al 2017;Tang et al 2017) and from ready to eat products (Wang et al 2017;Islam et al 2019).…”

“…However, MRSA has been also found associated with community setting (CA-MRSA) and with livestock (LA-MRSA) (Pantosti 2012). Recently, MRSA has been isolated in various types of food products, including raw milk, dairy products (Carfora et al 2015;Caruso et al 2016;Parisi et al 2016;Basanisi et al 2017;Giaciniti et al 2017;Titouche et al 2019;Papadopoulos et al 2019a) and meat (Tang et al 2017;Thapaliya et al 2017). Transmission of zoonotic MRSA to humans can occur via either animal contact or contaminated food (Oniciuc et al 2017).…”

“…In Algeria, the proportion of MRSA demonstrated a high increase in the community and healthcare settings; the European clone ST80-IV, producer of the Panton-Valentine Leukocidin (PVL), has being detected (Antri et al 2011;Djahmi et al 2013;Chaalal et al 2018). A previous study of our group (Titouche et al 2019) was focusing on analysing dairy products obtained in 2014-2015, in which MRSA was isolated from some raw milk and acidified milk samples. In the present work, the objectives were as follows: (i) to determine the prevalence of S. aureus in food products obtained during 2017-2018 (dairy and meat products, among others), (ii) to evaluate the content in enterotoxin genes and (iii) to characterize the MRSA isolates by spa typing, multilocus sequence typing (MLST) and antimicrobial resistance susceptibility testing.…”