| More

Prevalence and antimicrobial susceptibility of Enterococcus spp. in ready-to-eat salads (dips), the environment and the personnel of a salad processing plant in Northern Greece

Views: 390 Downloads: 230


A total of 225 samples from the dips (cheese, roe, egg plant and tzatziki dip), the environment and the handlers of a salad manufacturing plant in Northern Greece were examined for the presence and antibiotic susceptibility of Entervcocccus spp. Enterococcus faecium was the isolated species from 12% of the samples. 38.1% and 15% of egg plant and cheese dip samples were positive, respectively. Among the dip ingredients, 30% of mayonnaise, 20% of feta cheese and 10% of myzithra were positive. Positive were, also, 8.6 % of the environmental samples, 20% from handlers' skirts, 20% from handlers' gloves and 16.7% from their nasal cavity. All isolates were sensitive to glycopeptides (vancomycin and teicoplanin). Isolates from handlers' nasal cavities were resistant to penicillin and ampicillin, while one of them was, also, resistant to chloramphenicol. All isolates from the environment, the dips and their ingredients were susceptible to these three antibiotics, but they presented resistance to more than 3 antibiotic categories. Ready-to-eat foods may be potential source of contamination to humans of multidrug resistant enterococci. Further research is needed to elucidate their epidemiology in these foods.



Enterococcus spp.; antimicrobial susceptibility; ready-to-eat dips; environment

Full Text:



Barbosa J, Ferreira V, Teixeira Ρ (2009) Antibiotic susceptibility of enterococcci isolated from traditional fermented meat products. Food Microbiol 26:527-532.

Bates J (1997) Epidemiology of vancomycin-resistant enterococci in the community and the relevance to farm animals to human infections. J Hospital Infection 37: 89-101.

Bager F, Madsen M, Christensen J, Aarestrup FM (1997) Avoparcin used as a growth promoter is associated with the occurrence of vancomycin resistant Enterococcus faecium on Danish poultry and pig farms. Prev Vet Med 31: 95-112.

Ben Omar N, Castro A, Lucas R, Abriouel H, Yousif NMK, Franz CMAP, Holzapfel, WH, Perez-Pulito R, MartineZ-Canamero M, Galvez A (2004) Functional and safety aspects of enterococci

isolated from different Spanish foods System. Appi Microbiol 27:118-130.

Boyle JM, Soumakis, SA, Rendo A, Herrington JA, Gianarakis DG, Thurberg BE, Painter BG (1993) Epidemiologic analysis and genotypic characterization of a nosocomial outbreak of vancomycin-resistant enterococci. J Clinical Microbiol 31:1280-1285.

Canzek Majhenij A, Rigelj I, Perko Β (2005) Enterococci from Tolmic cheese: population structure, antibiotic susceptibility and incidence of virulence determinants. J Food Microbiol 2:239-244.

Centeno JA, Mendez S, Podriguez-Otero JL (1996) Main microbial flora present as natural starters in Cebreiro raw cow's milk cheese (Northwest Spain). Int J Food Microbiol 33:307-313.

Chatterjee I, Iredell JR, Woods M, Lipmann J (2007) The implications of enterococci in the intensive care unit. Crit Care Resusc 9:69-75.

Chingwaru W, Mpuchane SF, Cashe Β A (2003) Enterococcus faecalis and Enterococcus faecium isolates from milk, beef and chicken and their antibiotic resistance. J Food Prot 66:931-936.

Citak S, Yucel N, Orhan S (2004) Antibiotic resistance and incidence of Enterococcus in Turkish white cheese. Int J Dairy Technol 57:27-31.

Clinical and Laboratory Standards Institute/CCLI (2009) Performance Standards for Antimicrobial Susceptibility Testing. Nineteenth informational supplement. M100-S19. CLSI, Wayne, PA.

Consentino S, Pisano MB, Corda A, Fadda ME, Piras C (2004) Genotypic and technological characterization of enterococci isolated from artisanal Fiore Sardo cheese. J Dairy Res 71:444-450.

Coppola S, Parente E, Dumonter S, La Peccerella A (1988) The microflora of natural whey cultures utilized as starter cultures in the manufacture of Mozzarella cheese from water-buffalo milk. Lait 68:295-310.

Franz CMAP, Holzapfel WH, Stiles ME (1999) Enterococci at the crossroad of food safety. Int J Food Microbiol 47:1-24.

Franz CMAP, Muscholl-Silberhorn AN, Yousif NMK, Vancanneyt M, Swings J, Holzapfel WH (2001) Incidence of virulence factors and antibiotic resistance among enterococci isolated from food. Appi Environ Microbiol 65:2385-4389.

Giraffa G, Olivari AM, Neviani E (2000) Isolation of vancomycin - resistant Enterococcus faecium from Italian cheese. Food Microbiol 17:671-677.

Godfree AF, Kay D, Wyer MD (1997) Faecal streptococci as indicators of faecal contamination in water. J Appi Microbiol Symposium Supplement 83:15-115.

Gomes BC, Esteves CT, Palazzo ICV, Darini ALC, Felis GÈ, Sechi LA, Franco BDGM, De Martini ECP (2008) Prevalence and characterization of Enterococcus spp. isolated from Brazilian foods. Food Microbiol 25:668-675.

Klein C, Pack A, Bonaparte C, Reuter G (1998) Taxonomy and physiology of probiotic lactic acid bacteria. Int J Food Microbiol 41:103-12.

Koluman A, Akan LS, Çakiroglu FP (2009) Occurrence and antimicrobial resistance of enterococci in retail foods. Food Control 20:281-283.

Litopoulou-Tzanetakis E, Tzanetakis N, Vafopoulou-Mastrojannaki A (1993) Effect and type of lactic starter on microbiological, chemical and sensory characteristics of feta cheese. Food Microbiol 10:31-41.

Lopes MF, Ribeiro T, Martins MP, Tenereiro R, Crespo MT (2003) Gentamicin resistance in dairy and clinical enterococcal isolates and in reference strains. J Antimicrob Chemother 52:214-219.

Lu HZ, Weng XH, Li H, Yin YK, Pang MY, Tang YW (2002) Enterococcus faecium-related outbreak with molecular evidence of transmission from pigs to humans. J Clinic Microbiol 40:913-917.

Majhenic AC, Rogelj I, Perko Β (2005) Enterococcci from Tolminc cheese: population, structure, antibiotic susceptibility and incidence of virulence determinants. Int J Food Micriobiol 102:239-244.

Maniatis AN, Pournaras S, Kanellopoulou M, Kontos F, Dimitroulia E, Papafrangas E, Tsakris A (2001) Dissemination of clonally unrelated erythromycin- and glycopeptide-resistant Enterococcus faecium isolates in a tertiary Greek hospital. J Clinic Microbiol 39:4571-4574.

Mannu L, Paba A, Daga E, Comunian R, Zanetti S, Dupre I, Sechi LA (2003) Comparison of the incidence of virulence determinants and antibiotic resistance between Enterococcus faecium strains of dairy, animal and clinical origin. J Food Microbiol 88:385-408.

Messi Ρ, Guerrieri E, de Niederhäusern S, Sabia C, Bondi M (2006) Vancomycin-resistant enterococcci (VRE) in meat and environmental samples. Int J Food Microbiol 107:218-222.

Metzidie E, Manolis EN, Pournaras W, Sofianou D, Tsakris A (2006) Spread of an unusual penicillin- and imipenem-resistant butampicillin-susceptible phenotype among Enterococcus faecalis clinical isolates. J Antimicrob Chemother 57:158-60.

Murray BE (1990) The life and times of the enterococci. Clinic Microbiol Rev 3:46-65.

Noble WG, Virani Z, Crée RGA (1992) Co-transfer of vancomycin and other resistance genes to Enterococcus faecalis NCTC 12201 to Staphylococcus aureus. FEMS Microbiology Letters 93:195-198.

Ogier JK, Serror Ρ (2008) Safety assessment of dairy microorganisms: The Enterococcus genus. J Food Microbiol 126:291-301.

Pavia M, Carmel G, Nobbles A, Splatter L, Angellala I (2000) Vancomycin resistance and antibiotic susceptibility of enterococci in raw meat. J Food Prot 63:912-915.

Peters J, Mac K, Wischmann-Schauber H, Klein G, Ellebroek L (2003) Species distribution and antibiotic resistance patterns of enterococci isolated from food of animal origin in Germany. J Food Microbiol 88:311-314.

Pournaras S, Malamou-Lada H, Maniati M, Mylona-Petropoulou D, Vagiakou-Voudris H, Tsakris A, Maniatis AN (2004) Persistence of a clone of glycopeptide-resistant Enterococcus faecalis among patients in an intensive care unit of a Greek hospital. J Antimicrob Chemother 53:109-12.

Quednau M, Ahmè S, Petersson AC, Molin G (1998) Antibiotic resistant strains of Enterococcus isolated from Swedish and Danish retailed chicken and pork. J Appi Microbiol 84:1163-1170.

Sabia C, de Niederhäusern S, Guerrieri E, Messi P, Anacarso I, Manicardi G, Bondi M (2008) Detection of becteriocin production and virulence traits in vancomycin-resistant enterococcci of different sources. J Appi Microbiol 104:970-979.

Sarantinopoulos Ρ, Kalantzopoulos G, Tsakalidou E (2002) Effect of Enterococcus faecium on microbiological, physicochemical and sensory characteristics of Greek feta cheese. Int J Food Microbiol 76:93-105.

Teuber M, Perreten V, Wirchin GF (1996) Antibiotikum resistente Bakterien: Eine neue Dimension in der Lebensmitteltechnologie. Lebensmittel-Technologie 29:182-189.

Teuber M, Meile L, Schwarz F (1999) Acquired antibiotic resistance in lactic acid bacteria from food. Antonie Leeuwenhoek 76:115-137.

Tzanetakis Ν, Litopoulou-Tzanetaki Ε (1992) Changes in numbers and kinds of lactic acid bacteria in Feta and Teleme, two Greek cheeses from ewe's milk. J Dairy Sci 75:1389-1393.

Weigel LM, Clewel DB, Gill SR, Clark NC, Mcdougal LK, Flannagan SE (2003) Genetic analysis of a high-level vancomycin resistant isolate of Staphylococcus aureus. Science 302:1569-1571.

Van den Braak N, Van Belkum A, Van Keulen M, Viegenthart J, Verbrugh HA, Endtz HP (1998) Molecular characterization of vancomycin-resistant enterococci from hospitalized patients and

poultry products in the Netherlands. J Clin Microbiol 36:1927-1932.

Wilson IG, Mcafee GG (2002) Vancomycin-resistant Enterococcci in shellfish, unchlorinated waters and chicken. Int J Food Microbiol 79:143-151.


  • There are currently no refbacks.


Creative Commons License
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.