Multidrug-, methicillin-, and vancomycin-resistant Staphylococcus aureus isolated from ready-to-eat meat sandwiches: An ongoing food and public health concern

Mahros, Mahmoud Ahmed; Abd-Elghany, Samir Mohammed; Sallam, Khalid Ibrahim

doi:10.1016/j.ijfoodmicro.2021.109165

Cited by 52 publications

(33 citation statements)

References 40 publications

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“…These high resistance rates may be related to the use of antimicrobials for treating disease and as growth promoters or feed additives in livestock. In this study, the MDR isolate rate of S. aureus (92.5%) from retail pork was consistent with the report that indicated that 90.0% of the strains were isolated from ready-to-eat meat sandwiches in Egypt ( Mahmoud et al, 2021 ). However, this rate was higher than those reported for BTM (55.4%) and retail ready-to-eat foods (75.8%) in China ( Zhao et al, 2021 ; Yang et al, 2016 ).…”

Section: Discussionsupporting

confidence: 91%

Whole-Genome Epidemiology and Characterization of Methicillin-Susceptible Staphylococcus aureus ST398 From Retail Pork and Bulk Tank Milk in Shandong, China

Zhao

et al. 2021

Front. Microbiol.

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Staphylococcus aureus (S. aureus) is now regarded as a zoonotic agent. Methicillin-susceptible S. aureus (MSSA) ST398 is a livestock-associated bacterium that is most prevalent in China, but there are currently no data available for Shandong. Therefore, the aim of this study was to investigate the epidemiology and characterization of MSSA ST398 from retail pork and bulk tank milk (BTM) in Shandong. A total of 67 S. aureus isolates were collected from retail pork between November 2017 and June 2018. Among the isolates, high antimicrobial resistance rates were observed for penicillin (97.0%), and 92.5% of the isolates were multi-drug resistant (MDR). Eight sequence types (STs) were identified in the retail pork isolates, and the predominant type was ST15 (n=26), which was followed by ST398 (n=14). Staphylococcal protein A gene (spa) typing identified spa types t034 and t1255 in MSSA ST398 from retail pork. Using whole-genome sequencing analysis, we described the phylogeny of 29 MSSA ST398 isolates that were obtained from retail pork (n=14) and BTM (n=15). The phylogenetic tree showed that the MSSA ST398 isolates from different sources had the same lineage. Among the 29 MSSA ST398 isolates, five resistance genes were detected, and all isolates carried DHA-1. Fifteen toxin genes were detected, and all isolates carried eta, hla, and hlb. In conclusion, this study found that a high risk for MSSA ST398 was present in retail pork and BTM. These findings have major implications for how investigations of MSSA ST398 outbreaks should be conducted in the One-Health context.

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Section: Discussionsupporting

confidence: 91%

Whole-Genome Epidemiology and Characterization of Methicillin-Susceptible Staphylococcus aureus ST398 From Retail Pork and Bulk Tank Milk in Shandong, China

Zhao

et al. 2021

Front. Microbiol.

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“…Staphylococcus aureus colonizes the nasopharynx of asymptomatic carriers leading to the contamination of the hands of food handlers [13,14]. Antimicrobial resistant strains of S. aureus have been detected in food [12,15,16] and foodborne outbreaks of S. aureus have been related with post-process food contamination by the hands of food handlers [17].…”

Section: Introductionmentioning

confidence: 99%

Microbiological Contamination in Different Food Service Units Associated with Food Handling

et al. 2021

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Background: A microbiological analysis of samples taken from hands of food handlers and utensils/crockery in food service units was used to assess the risk of food contamination. We aimed to assess indicators of microbiological contamination in different food service units. Methods: We used data for an official inspection proposal (2018–2019) in different food service units serving a district in Northeast Portugal. We showed the proportion of positive samples for each microorganism assessed in samples taken from hands and kitchen utensils/crockery. Results: Out of 471 samples taken from hands of food handlers, 26.8% (n = 126) were classified as “unsatisfactory” due to the presence of at least Escherichia coli, Staphylococcus aureus and/or total and fecal coliforms. Such a proportion varied according to the type of food service unit with a higher proportion being observed in Canteens (40.0%) and in Retirement Home/Day Care Centers (37.8%). More than one third of 649 samples taken from kitchen utensils/crockery were classified as “unsatisfactory” (n = 181; 27.9%) or “bad” (n = 49; 7.6%). There were significant differences in these proportions across food service units, with a higher proportion of “unsatisfactory” samples being observed in Fishmongers and Butcher Shops/Charcuteries (50.0% and 45.1%, respectively), while a higher proportion of “bad” samples was observed in both Pastry/Bakery and Fishmonger establishments (33.3%), followed by Butcher Shops/Charcuteries (14.1%). Conclusions: Our results emphasize the need of awareness of hygiene practices among food handlers of different food service units, particularly in Fishmongers, Pastry/Bakery establishments and Butcher Shops/Charcuteries, highlighting the need of a periodic hygienic evaluation.

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“…The differences in the microbiological quality of raw ingredient, the utensils and equipment used for food preparation, cooking, the presence of seasoning ingredients, isolation methods may contribute to the observed differences in the bacterial detection rate (Daelman et al, 2013;Wang et al, 2014). Our study reported a higher frequency of MRSA isolates from the examined COPS isolates recovered from shawarma and burger sandwiches (100%) than that obtained previously in beef burger and hot dog sandwiches (22.2%) (Mahros et al, 2021) and in other RTE meat products (25%) (Saad et al, 2019). This suggests the increased occurrence of MRSA in this kind of RTE meat.…”

Section: Discussionmentioning

confidence: 43%

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

et al. 2022

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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.

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Multidrug-, methicillin-, and vancomycin-resistant Staphylococcus aureus isolated from ready-to-eat meat sandwiches: An ongoing food and public health concern

Cited by 52 publications

References 40 publications

Whole-Genome Epidemiology and Characterization of Methicillin-Susceptible Staphylococcus aureus ST398 From Retail Pork and Bulk Tank Milk in Shandong, China

Whole-Genome Epidemiology and Characterization of Methicillin-Susceptible Staphylococcus aureus ST398 From Retail Pork and Bulk Tank Milk in Shandong, China

Microbiological Contamination in Different Food Service Units Associated with Food Handling

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

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