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Enterococci from Appenzeller and Schabziger Raw Milk Cheese: Antibiotic Resistance, Virulence Factors, and Persistence of Particular Strains in the Products

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Enterococci from Appenzeller and Schabziger Raw Milk Cheese: Antibiotic Resistance, Virulence Factors, and Persistence of Particular Strains in the Products 450 Journal of Food Protection, Vol. 70, No. 2, 2007, Pages 450–455 Copyright ᮊ, International Association for Food Protection Enterococci from Appenzeller and Schabziger Raw Milk Cheese: Antibiotic Resistance, Virulence Factors, and Persistence of Particular Strains in the Products S. P. TEMPLER AND A. BAUMGARTNER* Section of Microbiology and Biotechnology, Swiss Federal Office of Public Health, Schwarzenburgstrasse 165, 3097 Liebefeld, Switzerland MS 06-298: Received 31 May 2006/Accepted 29 September 2006 Downloaded from http://meridian.allenpress.com/jfp/article-pdf/70/2/450/1678809/0362-028x-70_2_450.pdf by guest on 25 September 2021 ABSTRACT Enterococci are natural residents of human and animal intestinal tracts, and grow to high numbers in a variety of cheeses. The aim of this study was to determine the diversity of enterococci in two types of artisanal raw milk cheese (Schabziger and Appenzeller) and to investigate whether particular strains with triple resistance against chloramphenicol (Chl), tetracycline (Tet), and erythromycin (Ery) persist in the production system. Of 46 cheese samples, a total of 312 Enterococcus strains were isolated over a 5-month period on selective agar plates containing Chl, Tet, or, Ery. Enterococcus faecalis was the predominant species (80.7%), followed by Enterococcus faecium (5.1%), and Enterococcus durans (11.7%). According to the phenotypic resistance patterns, a selection of 150 strains was analyzed with PCR for the presence of genes encoding resistance to Ery (ereA, ereB, mphA, ermA, ermB, ermC, mrsA/mrsB, mefA/mefE), and Tet (tetM, tetL). Because virulence factors have been linked to the pathogenicity of enterococci, the strain selection was also tested for the presence of the following virulence factors: Agg, GelE, Cyl, Esp, EfaAfs, EfaAfm, Cpd, Cob, and Ccf. All tested strains contained at least two of the nine virulence genes taken into analysis. Pulsed-field gel electrophoresis patterns of the isolates showed a limited persistence of several strains over a period of 1 to 2 months in Schabziger, and more than 2 months in Appenzeller. Finally, the enterococcal flora in the two types of cheeses seems to be rather unrelated. Within 150 strains from 25 different cheese samples (11 Appenzeller and 14 Schabziger), 41 pulsed-field gel electrophoresis patterns could be identified, and only 1 of these was found in enterococci from both types of cheese. Enterococci are found in a variety of cheeses made associated protein that is involved in the immune evasion. from raw or pasteurized cow’s milk (3, 13). For a long time, It is possible that esp and cylABM genes are associated on the presence of these bacteria in foods was associated with a pathogenicity island (25). Agg is a surface-localized pro- fecal contamination, but nowadays they are considered as tein encoded by pheromone-responsive, self-transmissible normal part of food microflora (19). Enterococci seem to plasmids, which mediates binding of donor bacterial cells improve the flavor development and cheese quality (13). with plasmid-free recipients, allowing efficient conjugal Because of antilisterial activity based on bacteriocin pro- transfer in a liquid environment (9). Another adhesin-like duction, they are also used in food preservation (13, 14, virulence factor is the E. faecalis and E. faecium antigen A 16). (EfaAfs and EfaAfm, respectively) that are expressed in the In spite of the beneficial activities of enterococci, they serum (21). Gelatinase is an extracellular metalloendopep- have become important over the past decade as one of the tidase that hydrolyzes gelatin, collagen, hemoglobin, and most frequently encountered nosocomial pathogens and ap- other bioactive compounds (31). The sex pheromones (Cpd, pear to have increasing resistance to antimicrobials (20, 22, Cob, Ccf ) are thought to be involved in eliciting an inflam- 23). An even greater threat is the transfer of resistance to matory response. These pheromones are chemotactic for vancomycin or other antimicrobials within and over the human leukocytes and induce production and secretion of species border (9–11, 20). To cause infection, enterococci lysosomal enzymes and thereby facilitate conjugation (8). must be able to colonize the host tissue, resist host-specific Previous studies showed that enterococci can be found and -unspecific defense mechanisms, and cause pathologi- in a variety of ready-to-eat products in Switzerland (3, 5). cal changes. Thus they have to be virulent, and virulence Further, in a high amount of enterococcal isolates from raw factors including cytolysin (CylABM), enterococcal surface milk cheese, triple resistance against chloramphenicol protein (Esp), aggregation substance (Agg), and gelatinase (Chl), tetracycline (Tet), and erythromycin (Ery) could be (GelE) should be taken into consideration as well (12, 13, demonstrated. The aim of this study was to determine the 22, 25). CylABM causes ruptures of a variety of mem- diversity of enterococci in two types of artisan raw milk branes, including those of bacterial cells, erythrocytes, and cheese (Schabziger and Appenzeller), and to investigate other mammalian cells (29). Esp (30) produces a cell wall– whether particular strains with triple resistance against Chl, * Author for correspondence. Tel: ϩ41 31 322 95 82; Fax: ϩ41 31 322 Tet, and Ery persist in the production system. 95 74; E-mail: [email protected]. Appenzeller is a hard-type cheese, produced from raw J. Food Prot., Vol. 70, No. 2 PERSISTENCE OF ANTIBIOTIC-RESISTANT ENTEROCOCCI IN RAW MILK CHEESE 451 cow’s milk. Milk is inoculated with a starter culture con- Phenotypic and genotypic assessment of virulence traits. taining lactic acid bacteria. The milk coagulation is started The phenotypic assessment of hemolysis was examined by streak- with addition of rennet. Cheese is normally ripened for ing the isolates on 5% sheep blood Colombia agar (bioMe´rieux) Њ about 3 to 4 months. Schabziger cheese (also known as and incubated at 37 C for 24 h in order to determine the hemolytic Sapsago) is a creamery, hard, fat-free, pungent grating activity. The gelatinase activity of the isolates was tested with brain heart infusion broth (Oxoid) containing 12% of gelatin. The cheese. It is spiced with fenugreek. During the ripening brain heart infusion–gelatin broth was liquefied at 37ЊC and in- process the cheese is grated to avoid formation of rind. oculated with the isolates. After incubation (37ЊC, 48 h) the tubes Schabziger cheese is produced in only one production plant were kept at 4ЊC for 30 min. Gelatinase-positive isolates could be in Switzerland and is therefore an ideal model system to identified by the liquid medium. PCR assays were performed us- show persistence of particular strains of enterococci. ing pairs of previously reported primers (12) for the detection of the following genes: agg, gelE, cylM, cylB, cylA, esp, efaAfs, MATERIALS AND METHODS efaAfm, cpd, cob, and ccf. Cheese sampling and isolation of enterococci. Over a pe- Downloaded from http://meridian.allenpress.com/jfp/article-pdf/70/2/450/1678809/0362-028x-70_2_450.pdf by guest on 25 September 2021 PCR assay. For all detection assays, a common PCR core riod of 5 months, a cheese sample of every new batch production mix (total volume of 50 ␮l) was used consisting of 1ϫ PCR buffer of Schabziger cheese (21 samples) and Appenzeller cheese (26 (Promega, Madison, Wis.), 200-␮M concentrations of deoxynu- samples) was analyzed. The samples were diluted 1:10 in 0.85% cleoside triphosphates (Promega), 1 U of Taq DNA polymerase (wt/vol) NaCl plus 0.01% (wt/vol) tryptone casein peptone (pH (Promega), 4 mM MgCl , and 20 pmol of the corresponding prim- 7.0) and homogenized for 2 min in a laboratory blender (Stom- 2 ers (Thermo Electron GmbH, Ulm, Germany). A 50-ng portion of acher 400, Seward, PBI International, Milano, Italy), and 100 ␮l intact total DNA was used as PCR template. of a 10-fold dilution series were spread plated on kanamycin aes- culin azide agar base (Oxoid, Ltd., Hampshire, England) to de- PFGE typing. The chromosomal DNA was prepared as pre- termine the number of enterococci per gram of product. To deter- viously described (4) by growing the cells on brain heart infusion mine the number of Chl-, Ery-, and Tet-resistant enterococci per agar for 48 h at 37ЊC. Cells were suspended in 10 mM Tris–100 gram of product, 100 ␮l of a 10-fold dilution series was spread mM EDTA, pH 8.0 (TE-100 buffer), and consequently the sus- plated on kanamycin aesculin azide agar base containing 20 ␮g/ pension’s OD was adjusted to 2.5. This suspension was mixed ml of Chl, 10 ␮g/ml of Ery, or 10 ␮g/ml of Tet. Plates were 600 with an equal volume of 1.5% SeaKem Gold Agarose (Cambrex incubated at 37ЊC for 48 h. Bio Science Rockland, Rockland, Maine) in 10 mM Tris–1 mM Up to 10 colonies were randomly selected from antibiotic- EDTA, pH 8.0 (TE-buffer), to pour plugs. The solidified agar containing agar plates used for plate counting of a cheese sample. plugs were transferred in 1.5 ml TE-100 buffer with 25 mg/ml The colonies were purified twice on brain heart infusion agar (Ox- lysozyme (Sigma-Aldrich, Buchs, Switzerland) and rotated over- oid). The strain labeling was done as follows. The cheese type night at 10 rpm (Hybaid Mini 10, MWG-Biotech, Ebersber, Ger- was abbreviated with ‘‘SCH’’ for Schabziger and ‘‘APP’’ for Ap- many) at 37ЊC. After washing the plugs twice in TE-100 buffer penzeller, respectively. This abbreviation was followed by the iso- for 15 min, 1.5 ml of 0.5 M EDTA–1% N-lauroylsarcosine (pH late number (consecutively numbered) and the hyphenated cheese 8.0) and 2 mg/ml of proteinase K (Roche, Basel, Switzerland) sample number (example: SCH003-1, indicating the third entero- were added and incubated overnight at 50ЊC, under rotation.
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