Antibiotic Resistance Traits and Molecular Subtyping of <i>Staphylococcus aureus</i> Isolated from Raw Sheep Milk Cheese

Spanu, Vincenzo; Scarano, Christian; Cossu, F; Pala, Carlo; Spanu, Carlo; Santis, E.P.L. De

doi:10.1111/1750-3841.12590

Cited by 25 publications

(27 citation statements)

References 46 publications

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“…appeared mostly at the end of ripening, suggesting that staphylococci develop when the cheese matrix approaches the neutrality (pH 7.0). Antibiotic resistances in S. aureus, coagulase-negative staphylococci and other staphylococci species has been repeatedly reported (Jamali et al, 2014;Spanu et al, 2014;Wang et al, 2012;Resch et al, 2008). However, the PCR-DGGE findings of this study suggest that the major carriers of antibiotic resistance proved to be members of the species groups Staphylococcus simulans and Staphylococcus saprophyticus.…”

Section: Discussioncontrasting

confidence: 57%

Diversity and dynamics of antibiotic-resistant bacteria in cheese as determined by PCR denaturing gradient gel electrophoresis

Flórez

Mayo

2015

International Journal of Food Microbiology

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This work reports the composition and succession of tetracycline- and erythromycin-resistant bacterial communities in a model cheese, monitored by polymerase chain reaction denaturing gradient gel electrophoresis (PCR-DGGE). Bacterial 16S rRNA genes were examined using this technique to detect structural changes in the cheese microbiota over manufacturing and ripening. Total bacterial genomic DNA, used as a template, was extracted from cultivable bacteria grown without and with tetracycline or erythromycin (both at 25 μg ml(-1)) on a non-selective medium used for enumeration of total and viable cells (Plate Count agar with Milk; PCA-M), and from those grown on selective and/or differential agar media used for counting various bacterial groups; i.e., lactic acid bacteria (de Man, Rogosa and Sharpe agar; MRSA), micrococci and staphylococci (Baird-Parker agar; BPA), and enterobacteria (Violet Red Bile Glucose agar; VRBGA). Large numbers of tetracycline- and erythromycin-resistant bacteria were detected in cheese samples at all stages of ripening. Counts of antibiotic-resistant bacteria varied widely depending on the microbial group and the point of sampling. In general, resistant bacteria were 0.5-1.0 Log10 units fewer in number than the corresponding susceptible bacteria. The PCR-DGGE profiles obtained with DNA isolated from the plates for total bacteria and the different bacterial groups suggested Escherichia coli, Lactococcus lactis, Enterococcus faecalis and Staphylococcus spp. as the microbial types resistant to both antibiotics tested. This study shows the suitability of the PCR-DGGE technique for rapidly identifying and tracking antibiotic resistant populations in cheese and, by extension, in other foods.

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Section: Discussioncontrasting

confidence: 57%

Diversity and dynamics of antibiotic-resistant bacteria in cheese as determined by PCR denaturing gradient gel electrophoresis

Flórez

Mayo

2015

International Journal of Food Microbiology

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“…The presence of CPS in cheeses made from pasteurized milk may indicate a failure in pasteurization or recontamination after pasteurization due to insufficient hygienic and sanitary practices (O'Brien et al, 2009). High counts of CPS in raw milk cheese are expected because that milk can be contaminated directly from the production environment, infected animal, or food handler (Spanu et al, 2014). Variable results have been observed by other authors in samples obtained in Brazil such as 21.0% in Bahia and 31.2% in Pernambuco (Evêncio-Luz et al, 2012) and 54.2% in Goiás (André et al, 2008).…”

Section: Coagulase-positive Staphylococcimentioning

confidence: 99%

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

Ferreira

Bernardo

Neves

et al. 2016

Journal of Dairy Science

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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.

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“…Coagulase‐negative staphylococci and S. aureus were also identified in this study. These species are considered significant pathogens both in human and veterinary medicine due to their pathogenic potential (Fontes and others ; Spanu and others ). Several characteristics may contribute to virulence in staphylococci, such as the ability to produce extracellular polymers, enterotoxins, hemolysins, hydrolytic enzymes, and structural components that may impair the host's immune system (Piette and Verschraegen ).…”

Section: Resultsmentioning

confidence: 99%

“…Among these microorganisms, especially Gram positive cocci (GPC) such as Enterococcus spp. and Staphylococcus spp., have been frequently found in cheese (Pesavento and others ; Spanu and others ). Although sanitary legislation considers some species as quality indicators, others that are also potentially pathogenic are neglected, especially considering the emergence of the antimicrobial resistance phenomena (Fontes and others ).…”

Section: Introductionmentioning

confidence: 94%

Antimicrobial‐Resistance Genetic Markers in Potentially Pathogenic Gram Positive Cocci Isolated from Brazilian Soft Cheese

Resende

Fontes

Ferreira-Machado

et al. 2018

Journal of Food Science

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Although most Brazilian dairy products meet high technological standards, there are quality issues regarding milk production, which may reduce the final product quality. Several microbial species may contaminate milk during manufacture and handling. If antimicrobial usage remains uncontrolled in dairy cattle, the horizontal transfer of antimicrobial resistance genes in foodstuffs may be of particular concern for both food producers and dairy industry. This study focused on the evaluation of putative Gram positive cocci in Minas cheese and of antimicrobial and biocide resistance genes among the isolated bacteria. Representative samples of 7 different industrially trademarked Minas cheeses (n = 35) were processed for selective culture and isolation of Gram positive cocci. All isolated bacteria were identified by DNA sequencing of the 16S rRNA gene. Antimicrobial resistance genes were screened by PCR. Overall, 208 strains were isolated and identified as follows: Enterococcus faecalis (47.6%), Macrococcus caseolyticus (18.3%), Enterococcus faecium (11.5%), Enterococcus caseliflavus (7.7%), Staphylococcus haemolyticus (7.2%), Staphylococcus aureus (4.3%), Staphylococcus epidermidis (2.9%), and Enterococcus hirae (0.5%). The genetic markers mecA (78.0%) and smr (71.4%) were the most prevalent, but others were also detected, such as blaZ (65.2%), msrA (60.9%), msrB (46.6%), linA (54.7%), and aacA-aphD (47.6%). The occurrence of opportunist pathogenic bacteria harboring antimicrobial resistance markers in the cheese samples are of special concern, since these bacteria are not considered harmful contaminating agents according to the Brazilian sanitary regulations. However, they are potentially pathogenic bacteria and the cheese may be considered a reservoir for antimicrobial resistance genes available for horizontal transfer through the food chain, manufacturing personnel and consumers.

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Antibiotic Resistance Traits and Molecular Subtyping of Staphylococcus aureus Isolated from Raw Sheep Milk Cheese

Abstract: The present research contributes to increase the knowledge on the diffusion of antibiotic resistant S. aureus strains isolated from raw sheep milk cheeses. These can be regarded as a vehicle for the introduction of strains of animal origin to humans through food.

Cited by 25 publications

References 46 publications

Diversity and dynamics of antibiotic-resistant bacteria in cheese as determined by PCR denaturing gradient gel electrophoresis

Diversity and dynamics of antibiotic-resistant bacteria in cheese as determined by PCR denaturing gradient gel electrophoresis

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

Antimicrobial‐Resistance Genetic Markers in Potentially Pathogenic Gram Positive Cocci Isolated from Brazilian Soft Cheese

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