Advanced SearchSearch Tips
Characterisation of Phenotypic and Genotypic Antibiotic Resistance Profile of Enterococci from Cheeses in Turkey
facebook(new window)  Pirnt(new window) E-mail(new window) Excel Download
 Title & Authors
Characterisation of Phenotypic and Genotypic Antibiotic Resistance Profile of Enterococci from Cheeses in Turkey
Kurekci, Cemil; Onen, Sevda Pehlivanlar; Yipel, Mustafa; Aslantas, Ozkan; Gundogdu, Aycan;
  PDF(new window)
The aim of this study was to determine the prevalence of enterococci in cheese samples and to characterize their antimicrobial resistance profiles as well as the associated resistance genes. A total of 139 enterococci were isolated from 99 cheese samples, the isolates were identified as E. faecalis (61.2%), E. faecium (15.1%), E. gallinarum (12.9%), E. durans (5.0%), E. casseliflavis (2.9%) and E. avium (2.9%). The most frequent antimicrobial resistance observed in enterococci isolates was to lincomycin (88.5%), followed by kanamycin (84.2%), gentamycin (low level, 51.1%), rifampin (46.8%) and tetracycline (33.8%). Among the isolates, the frequencies of high level gentamycin and streptomycin resistant enterococci strains were 2.2% and 5.8%, respectively. Apart from the mentioned antibiotics, low levels of resistance to ciprofloxacin, erythromycin and chloramphenicol were found. Moreover no resistance was observed against penicillin and ampicillin. The antimicrobial resistance genes including tetM, tetL, ermB, cat, aph(3’)-IIIa, ant(6)-Ia and aac(6’)-Ieaph(2”)-Ia were found in enterococci from Turkish cheese samples. In the current study, we provided data for antibiotic resistance and the occurrence of resistance genes among enterococci. Regulatory and quality control programs for milk and other dairy products from farms to retail outlets has to be established and strengthened to monitor trends in antimicrobial resistance among emerging food borne pathogens in Turkey.
enterococci;cheese;antimicrobial resistance;resistance genes;
 Cited by
Aarestrup, F. M., Agrees, Y., Gerner-Smith, P., Madsen, M., and Jensen, L. B. (2000) Comparison of antimicrobial resistance phenotypes and resistance genes in Enterococcus faecalis and Enterococcus faecium from humans in the community, broilers and pigs in Denmark. Diagn. Micr. Infec. Dis. 37, 127-137. crossref(new window)

Ahmadova, A., Todorov, S. D., Choiset, Y., Rabesona, H., Zadi, T. M., Kuliyev, A., Melo Franco, B. D. G., Chobert, J. M., and Thomas Haertlé, T. (2013) Evaluation of antimicrobial activity, probiotic properties and safety of wild strain Enterococcus faecium AQ71 isolated from Azerbaijani Motal cheese. Food Control 30, 631-641. crossref(new window)

Araoka, H., Kimura, M., and Yoneyama, A. (2011) A surveillance of high-level gentamicin-resistant enterococcal bacteremia. J. Infect. Chemother. 17, 433-434. crossref(new window)

Arias, C. A., Contreras, G. A., and Murray, B. E. (2010) Management of multidrug-resistant enterococcal infections. Clin. Microbiol. Infec. 16, 555-562. crossref(new window)

Aygun, A., Aslantas, O., and Oner, O. (2005) A survey on the microbiological quality of Carra, a traditional Turkish cheese. J. Food Eng. 66, 401-404. crossref(new window)

Borgen, K., Simonsen, G. S., Sundsfjord, A., Wasteson, Y., Olsvik, E., and Kruse, H. (2000) Continuing high prevalence of VanA-type vancomycin-resistant enterococci on Norwegian poultry farms three years after avoparcin was banned. J. Appl. Microbiol. 89, 478-485. crossref(new window)

Bortolaia, V., Mander, M., Jensen, L. B., Olsen, J. E., and Guardabassi, L. (2015) Persistance of vancomycin resistance in multiple clones of Enterococcus faecium isolated from Danish broilers 15 years after the ban of avoparcin. Antimicrob. Agents Chemother. 59, 2926-2929. crossref(new window)

Choi, J. M. and Woo, G. J. (2013) Molecular characterization of high-level gentamicin-resistant Enterococcus faecalis from chicken meat in Korea. Int. J. Food Microbiol. 165, 1-6. crossref(new window)

Çitak, S., Yucel, N., and Orhan, S. (2004) Antibiotic resistance and incidence of Enterococcus species in Turkish white cheese. Int. J. Dairy Technol. 57, 27-31. crossref(new window)

Clinical and Laboratory Standards Institute (CLSI) (2012) Performance Standards for Antimicrobial Susceptibility Testing; Twenty-second informational supplement. CLSI document, M100-S22, 32, 3. Retrieved August 05, 2015, from

Depardieu, F., Perichon, B., and Courvalin, P. (2004) Detection of the van alphabet and identification of Enterococci and Staphylococci at the species level by multiplex PCR. J. Clin. Microbiol. 42, 5857-5860. crossref(new window)

DiazGranados, C. A., Zimmer, S. M., Mitchel, K., and Jernigan, J. A. (2005) Comparison of mortality associated with vancomycin-resistant and vancomycin-susceptible enterococcal bloodstream infections: A meta-analysis. Clin. Infect. Dis. 41, 327-333. crossref(new window)

Foulquie, M. M. R., Sarantinopoulos, P., Tsakalidou, E., and DeVuyst, L. (2006) The role and application of enterococci in food and health. Int. J. Food Microbiol. 106, 1-24. crossref(new window)

Franz, C. M. A. P., Holzapfel, W. H., and Stiles, M. E. (1999) Enterococci at the crossroads of food safety. Int. J. Food Microbiol. 47, 1-24. crossref(new window)

Furlaneto-Maia, L., Rocha, K. R., Henrique, F. C., Giazzi, A., and Furlaneto, M. C. (2014) Antimicrobial resistance in Enterococcus sp. isolated from soft cheese in southern Brazil. Adv. Microbiol. 4, 175-181. crossref(new window)

Hammad, A. M., Hassan H. A., and Shimamoto, T. (2015) Prevalence, antibiotic resistance and virulence of Enterococcus spp. in Egyptian fresh raw milk cheese. Food Control 50, 815-820. crossref(new window)

Hammad, A. M., Shimamoto, T., and Shimamoto, T. (2014) Genetic characterization of antibiotic resistance and virulence factors in Enterococcus spp. from Japanese retail ready-toeat raw fish. Food Microbiol. 38, 62-66. crossref(new window)

Harada, K. and Asai, T. (2010) Role of antimicrobial selective pressure and secondary factors on antimicrobial resistance prevalence in Escherichia coli from food-producing animals in Japan. J. Biomed. Biotechnol. 2010. doi:10.1155/2010/180682. crossref(new window)

Jamet, E., Akary, E., Poisson, M. A., Chamba, J. F., Bertrand, X., and Serror, P. (2012) Prevalence and characterization of antibiotic resistant Enterococcus faecalis in French cheeses. Food Microbiol. 31, 191-198. crossref(new window)

Kim, Y. J., Kim, S. I., Kim, Y. R., Lee, J. Y., Park, Y. J., and Kang, M. W. (2012) Risk factors for vancomycin-resistant enterococci infection and mortality in colonized patients on intensive care unit admission. Am. J. Infect. Control 40, 1018-1019. crossref(new window)

Klare, I., Konstabel, C., Badstübner, D., Werner, G., and Witte, W. (2003) Occurrence and spread of antibiotic resistances in Enterococcus faecium. Int. J. Food Microbiol. 88, 269-290. crossref(new window)

Koluman, A., Akan, L. S., and Çakiroglu, F. P. (2009) Occurrence and antimicrobial resistance of enterococci in retail foods. Food Control 20, 281-283. crossref(new window)

Kos, V. N., Desjardins, C. A., Griggs, A., Cerqueira, G., van Tonder, A., Holden, M. T. G., Godfrey, P., Palmer, K. L., Bodi, K., Mongodin, E. F., Wortman, J., Feldgarden, M., Lawley, T., Gill, S. R., Haas, B. J., Birren, B., and Gilmore, M. S. (2012) Comparative genomics of vancomycin-resistant Staphylococcus aureus strains and their positions within the clade most commonly associated with methicillin-resistant S. aureus hospital-acquired infection in the United States. mBio. 3, e00112-12.

Leavis, H. L., Bonten, M. J., and Willems, R. J. (2006) Identification of high-risk enterococcal clonal complexes: Global dispersion and antibiotic resistance. Curr. Opin. Microbiol. 9, 454-460. crossref(new window)

Leclercq, R., Derlot, E., Duval, J., and Courvalin, P. (1988) Plasmid-mediated resistance to vancomycin and teicoplanin in Enterococcus faecium. New Engl. J. Med. 319, 157-161. crossref(new window)

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

Liu, Y., Liu, K., Lai, J., Wu, C., Shen, J., and Wang, Y. (2012) Prevalence and antimicrobial resistance of Enterococcus species of food animal origin from Beijing and Shandong province, China. J. Appl. Microbiol. 114, 555-563.

Malhotra-Kumar, S., Lammens, C., Piessens, J., and Goossens, H. (2005) Multiplex PCR for simultaneous detection of macrolide and tetracycline resistance determinants in streptococci. Antimicrob. Agents Chemother. 49, 4798-4800. crossref(new window)

Nieto-Arribas, P., Seseña, S., Poveda, J. M., Chicón, R., Cabezas, L., and Palop, L. (2011) Enterococcus populations in artisanal Manchego cheese: Biodiversity, technological and safety aspects. Food Microbiol. 28, 891-899. crossref(new window)

Olsen, R. H., Schønheyder, H. C., Christensen, H., and Bisgaard, M. (2012) Enterococcus faecalis of human and poultry origin share virulence genes supporting the zoonotic potential of E. faecalis. Zoonoses Public Hlth. 59, 256-263. crossref(new window)

Özmen Toğay, S., Çelebi Keskin, A., Açik, L., and Temiz, A. (2010) Virulence genes, antibiotic resistance and plasmid profiles of Enterococcus faecalis and Enterococcus faecium from naturally fermented Turkish foods. J. Appl. Microbiol. 109, 1084-1092. crossref(new window)

Pesavento, G., Calonico, C., Ducci, B., Magnanini, A., and Lo Nostro, A. (2014) Prevalence and antibiotic resistance of Enterococcus spp. isolated from retail cheese, ready-to-eat salads, ham, and raw meat. Food Microbiol. 41, 1-7. crossref(new window)

Treitman, A. N., Yarnold, P. R., Warren, J., and Noskin, G. A. (2005) Emerging incidence of Enterococcus faecium among hospital isolates (1993 to 2002). J. Clin. Microbiol. 43, 462-463. crossref(new window)

Tuncer, Y. (2009) Some technological properties of phenotypically identified enterococci strains isolated from Turkish tulum cheese. Afr. J. Biotechnol. 8, 7008-7016.

Uttley, A. H., Collins, C. H., Naidoo, J., and George, R. C. (1988) Vancomycin-resistant enterococci. Lancet 1, 57-58.

Vakulenko, S. B., Zervos, M. J., Donabedian, S. M., Lerner, S. A., Voskresenskiy, A. M., and Chow, J.W. (2003) Multiplex PCR for detection of aminoglycoside resistance genes in enterococci. Antimicrob. Agents Chemother. 47, 1423-1426. crossref(new window)

World Health Organization (WHO) (2011) Critically Important Antimicrobials for Human Medicine, third revision. WHO Advisory Group on Integrated Surveillance of Antimicrobial Resistance (AGISAR). WHO Press, Geneva, Switzerland.

Yilmaz, E. S., Aslantas, Ö., Pehlivanlar Önen, S, Türkyilmaz S., and Kürekci C. (2016) Prevalence, antimicrobial resistance and virulence traits in enterococci from food of animal origin in Turkey. LTW-Food Sci. Technol. 66, 20-26.