Research Article
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Screening of Antibiotic Resistance and Virulence Genes of Enterococcus spp. Strains Isolated from Urfa Cheese

Year 2022, Volume 28, Issue 2, 223 - 231, 25.04.2022
https://doi.org/10.15832/ankutbd.868213

Abstract

Enterococcus faecium, E. durans and E. faecalis species were isolated and identified from traditional Urfa cheese samples which were produced from unpasteurized raw milk. The enterococcal load of the cheese samples was between 4.4-5.6 log cfu g−1. High-level tetracycline, streptomycin, erythromycin, gentamycin, and penicillin resistance was determined in the enterococcal isolates. Multiple antibiotic resistance was also determined in E. faecalis (20.4%) and E. faecium (16.3%) strains. 36.7% of the enterococcal isolates were greater than 0.2 MAR index ratio in this study. The gelE and agg2 genes were found in 40 (81.63%) of the enterococcal isolates, whereas the vanB gene was found in 3 (6.12%) of the enterococcal isolates. The results indicate that the consumption of Urfa cheese, which is produced using raw milk, may have public health risk because of its antibiotic resistance characteristics and virulence genes of enterococcal biota.

References

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  • Calonico C, Pesavento G, Delfino V, Forni S & Lo Nostro A (2018). Prevalence of antibiotic resistance in enterococci: A 14 year survey. Journal of Food and Nutrition Research 6(10): 626-637.
  • Camara S P A, Dapkevicius A, Silva C C G, Malcata F X, Maria L N & Dapkevicius E (2020). Artisanal Pico cheese as reservoir of Enterococcus species possessing virulence and antibiotic resistance properties: implications for food safety, Food Biotechnology, 34(1): 25-41.
  • Citak S, Yucel N & Orhan S (2004). Antibiotic resistance and incidence of Enterococcus species in Turkish white cheese. International Journal of Dairy Technology, 57(1): 27-31.
  • Clinical and Laboratory Standards Institute (CLSI), 2017. Performance Standards for Antimicrobial Susceptibility Testing. 27th ed. CLSI supplement M100. Wayne, PA, USA.
  • Eaton T J & Gasson, M J (2001). Molecular screening of Enterococcus virulence determinants and potential for genetic exchange between food and medical isolates. Applied and Environmental Microbiology, 67 (4): 1628-1635.
  • Hammad A M, Hassan H A & Shimamoto T (2015). Prevalence, antibiotic resistance and virulence of Enterococcus spp. in Egyptian fresh raw milk cheese. Food Control, 50, 815-820.
  • Ispirli H, Demirbas F & Dertli E (2017). Characterization of functional properties of Enterococcus spp. isolated from Turkish white cheese. LWT - Food Science and Technology, 75: 358-365.
  • Jurkovic D, Krizkova L, Dusinsky R, Belicova A, Sojka M, Krajcovic J & Ebringer L (2006). Identification and characterization of enterococci from Bryndza cheese. Letters in Applied Microbiology, 42: 553–559.
  • Kirmaci H A (2016). Effect of wild strains used as starter cultures on free fatty acid profile of Urfa cheese. Polish Journal of Food Nutrition Science, 66(4): 303–310.
  • Kirmaci H A, Ozer B H, Akcelik M & Akcelik N (2016). Identification and characterisation of lactic acid bacteria isolated from traditional Urfa cheese. International Journal of Dairy Technology, 69(2): 301-307.
  • Krumperman P H (1983). Multiple antibiotic resistance indexing of Escherichia coli to identify high-risk sources of fecal contamination of food. Applied and Environmental Microbiology, 46(1): 165-170.
  • Kürekci C, Pehlivanlar Önen S, Yipel M., Aslantas Ö & Gündogdu A (2016). Characterisation of phenotypic and genotypic antibiotic resistance profile of enterococci from cheeses in Turkey. Korean Journal for Food Science of Animal Resources, 36(3): 352-358.
  • Mrkonjic Fuka M, Zgomba Maksimovic A, Tanuwidjaja I, Hulak N & Schloter M (2017). Characterization of enterococcal community isolated from an artisan Istrian raw milk cheese: Biotechnological and safety aspects. Food Technology and Biotechnology, 55 (3): 368–380.
  • Özdemir R & Tuncer Y (2020). Detection of antibiotic resistance profiles and aminoglycosidemodifying enzyme (AME) genes in high-level aminoglycoside-resistant (HLAR) enterococci isolated from raw milk and traditional cheeses in Turkey. Molecular Biology Reports, 47: 1703–1712.
  • Pasquaroli S, Di Cesare A, Vignaroli C, Conti G, Citterio B & Biavasco F (2014). Erythromycin- and copper-resistant Enterococcus hirae from marine sediment and co-transfer of erm(B) and tcrB to human Enterococcus faecalis. Diagnostic Microbiology and Infectious Disease 80: 26–28.
  • Reviriego C, Eaton T, Martín R, Jiménez E, Fernández L, Gasson M J & Rodríguez J M (2005). Screening of virulence determinants in Enterococcus faecium strains isolated from breast milk. Journal of Human Lactation, 21(2): 131-138.
  • Sanlibaba P & Senturk E (2018) Prevalence, characterization, and antibiotic resistance of enterococci from traditional cheeses in Turkey. International Journal of Food Properties, 21(1): 1955-1963.
  • Silvetti T, Morandi S & Brasca M (2019). Does Enterococcus faecalis from traditional raw milk cheeses serve as a reservoir of antibiotic resistance and pathogenic traits? Foodborne Pathogens and Disease, 16(5).
  • Terkuran M, Erginkaya Z, Unal E, Guran M, Kizilyildirim S, Ugur G & Koksal F (2014). The relationship between virulence factors and vancomycin resistance among Enterococci collected from food and human samples in Southern Turkey. Veterinary Journal of Ankara University, 61: 133-140.
  • Templer S P & Baumgartner A (2007). Enterococci from Appenzeller and Schabziger raw milk cheese: Antibiotic resistance, virulence factors, and persistence of particular strains in the products. Journal of Food Protection, 70 (2): 450–455.
  • Uraz, G, Coskun S & Ozer B (2008). Microflora and pathogen bacteria (Salmonella, Klebsiella, Yersinia, Pseudomonas, Aeromonas, Escherichia coli, Staphylococcus aureus) in Urfa cheese (a traditional white-brined Turkish cheese). Pakistan Journal of Nutrition, 7(5): 630-635.
  • Zdolec N, Dobranic V, Butkovic I, Koturic A, Filipovic I & Medvid V (2016). Antimicrobial susceptibility of milk bacteria from healthy and drug-treated cow udder. Veterinarski Archiv, 86(2): 163-172.

Year 2022, Volume 28, Issue 2, 223 - 231, 25.04.2022
https://doi.org/10.15832/ankutbd.868213

Abstract

References

  • Bouymajane A, Rhazi Filali F, Oulghazi S, Ed-Dra A, Benhallam F, El Allaoui A, Anissi J, Sendide K, Ouhmidou B & Moumni M (2018). Occurrence, molecular and antimicrobial resistance of Enterococcus spp. isolated from raw cow's milk trade by street trading in Meknes city, Morocco. Germs 8(2): 77–84.
  • Calonico C, Pesavento G, Delfino V, Forni S & Lo Nostro A (2018). Prevalence of antibiotic resistance in enterococci: A 14 year survey. Journal of Food and Nutrition Research 6(10): 626-637.
  • Camara S P A, Dapkevicius A, Silva C C G, Malcata F X, Maria L N & Dapkevicius E (2020). Artisanal Pico cheese as reservoir of Enterococcus species possessing virulence and antibiotic resistance properties: implications for food safety, Food Biotechnology, 34(1): 25-41.
  • Citak S, Yucel N & Orhan S (2004). Antibiotic resistance and incidence of Enterococcus species in Turkish white cheese. International Journal of Dairy Technology, 57(1): 27-31.
  • Clinical and Laboratory Standards Institute (CLSI), 2017. Performance Standards for Antimicrobial Susceptibility Testing. 27th ed. CLSI supplement M100. Wayne, PA, USA.
  • Eaton T J & Gasson, M J (2001). Molecular screening of Enterococcus virulence determinants and potential for genetic exchange between food and medical isolates. Applied and Environmental Microbiology, 67 (4): 1628-1635.
  • Hammad A M, Hassan H A & Shimamoto T (2015). Prevalence, antibiotic resistance and virulence of Enterococcus spp. in Egyptian fresh raw milk cheese. Food Control, 50, 815-820.
  • Ispirli H, Demirbas F & Dertli E (2017). Characterization of functional properties of Enterococcus spp. isolated from Turkish white cheese. LWT - Food Science and Technology, 75: 358-365.
  • Jurkovic D, Krizkova L, Dusinsky R, Belicova A, Sojka M, Krajcovic J & Ebringer L (2006). Identification and characterization of enterococci from Bryndza cheese. Letters in Applied Microbiology, 42: 553–559.
  • Kirmaci H A (2016). Effect of wild strains used as starter cultures on free fatty acid profile of Urfa cheese. Polish Journal of Food Nutrition Science, 66(4): 303–310.
  • Kirmaci H A, Ozer B H, Akcelik M & Akcelik N (2016). Identification and characterisation of lactic acid bacteria isolated from traditional Urfa cheese. International Journal of Dairy Technology, 69(2): 301-307.
  • Krumperman P H (1983). Multiple antibiotic resistance indexing of Escherichia coli to identify high-risk sources of fecal contamination of food. Applied and Environmental Microbiology, 46(1): 165-170.
  • Kürekci C, Pehlivanlar Önen S, Yipel M., Aslantas Ö & Gündogdu A (2016). Characterisation of phenotypic and genotypic antibiotic resistance profile of enterococci from cheeses in Turkey. Korean Journal for Food Science of Animal Resources, 36(3): 352-358.
  • Mrkonjic Fuka M, Zgomba Maksimovic A, Tanuwidjaja I, Hulak N & Schloter M (2017). Characterization of enterococcal community isolated from an artisan Istrian raw milk cheese: Biotechnological and safety aspects. Food Technology and Biotechnology, 55 (3): 368–380.
  • Özdemir R & Tuncer Y (2020). Detection of antibiotic resistance profiles and aminoglycosidemodifying enzyme (AME) genes in high-level aminoglycoside-resistant (HLAR) enterococci isolated from raw milk and traditional cheeses in Turkey. Molecular Biology Reports, 47: 1703–1712.
  • Pasquaroli S, Di Cesare A, Vignaroli C, Conti G, Citterio B & Biavasco F (2014). Erythromycin- and copper-resistant Enterococcus hirae from marine sediment and co-transfer of erm(B) and tcrB to human Enterococcus faecalis. Diagnostic Microbiology and Infectious Disease 80: 26–28.
  • Reviriego C, Eaton T, Martín R, Jiménez E, Fernández L, Gasson M J & Rodríguez J M (2005). Screening of virulence determinants in Enterococcus faecium strains isolated from breast milk. Journal of Human Lactation, 21(2): 131-138.
  • Sanlibaba P & Senturk E (2018) Prevalence, characterization, and antibiotic resistance of enterococci from traditional cheeses in Turkey. International Journal of Food Properties, 21(1): 1955-1963.
  • Silvetti T, Morandi S & Brasca M (2019). Does Enterococcus faecalis from traditional raw milk cheeses serve as a reservoir of antibiotic resistance and pathogenic traits? Foodborne Pathogens and Disease, 16(5).
  • Terkuran M, Erginkaya Z, Unal E, Guran M, Kizilyildirim S, Ugur G & Koksal F (2014). The relationship between virulence factors and vancomycin resistance among Enterococci collected from food and human samples in Southern Turkey. Veterinary Journal of Ankara University, 61: 133-140.
  • Templer S P & Baumgartner A (2007). Enterococci from Appenzeller and Schabziger raw milk cheese: Antibiotic resistance, virulence factors, and persistence of particular strains in the products. Journal of Food Protection, 70 (2): 450–455.
  • Uraz, G, Coskun S & Ozer B (2008). Microflora and pathogen bacteria (Salmonella, Klebsiella, Yersinia, Pseudomonas, Aeromonas, Escherichia coli, Staphylococcus aureus) in Urfa cheese (a traditional white-brined Turkish cheese). Pakistan Journal of Nutrition, 7(5): 630-635.
  • Zdolec N, Dobranic V, Butkovic I, Koturic A, Filipovic I & Medvid V (2016). Antimicrobial susceptibility of milk bacteria from healthy and drug-treated cow udder. Veterinarski Archiv, 86(2): 163-172.

Details

Primary Language English
Subjects Science
Journal Section Makaleler
Authors

Sine ÖZMEN TOĞAY> (Primary Author)
BURSA ULUDAĞ ÜNİVERSİTESİ, ZİRAAT FAKÜLTESİ, GIDA MÜHENDİSLİĞİ BÖLÜMÜ
0000-0002-8851-1803
Türkiye


Şeniz KARAYİĞİT This is me
İstanbul Medipol Üniversitesi Sağlık Bilimleri Fakültesi Beslenme ve Diyetetik Bölümü
0000-0001-7985-8963
Türkiye

Publication Date April 25, 2022
Application Date January 25, 2021
Acceptance Date April 16, 2021
Published in Issue Year 2022, Volume 28, Issue 2

Cite

Bibtex @research article { ankutbd868213, journal = {Journal of Agricultural Sciences}, eissn = {2148-9297}, address = {}, publisher = {Ankara University}, year = {2022}, volume = {28}, number = {2}, pages = {223 - 231}, doi = {10.15832/ankutbd.868213}, title = {Screening of Antibiotic Resistance and Virulence Genes of Enterococcus spp. Strains Isolated from Urfa Cheese}, key = {cite}, author = {Özmen Toğay, Sine and Karayiğit, Şeniz} }
APA Özmen Toğay, S. & Karayiğit, Ş. (2022). Screening of Antibiotic Resistance and Virulence Genes of Enterococcus spp. Strains Isolated from Urfa Cheese . Journal of Agricultural Sciences , 28 (2) , 223-231 . DOI: 10.15832/ankutbd.868213
MLA Özmen Toğay, S. , Karayiğit, Ş. "Screening of Antibiotic Resistance and Virulence Genes of Enterococcus spp. Strains Isolated from Urfa Cheese" . Journal of Agricultural Sciences 28 (2022 ): 223-231 <https://dergipark.org.tr/en/pub/ankutbd/issue/68966/868213>
Chicago Özmen Toğay, S. , Karayiğit, Ş. "Screening of Antibiotic Resistance and Virulence Genes of Enterococcus spp. Strains Isolated from Urfa Cheese". Journal of Agricultural Sciences 28 (2022 ): 223-231
RIS TY - JOUR T1 - Screening of Antibiotic Resistance and Virulence Genes of Enterococcus spp. Strains Isolated from Urfa Cheese AU - Sine Özmen Toğay , Şeniz Karayiğit Y1 - 2022 PY - 2022 N1 - doi: 10.15832/ankutbd.868213 DO - 10.15832/ankutbd.868213 T2 - Journal of Agricultural Sciences JF - Journal JO - JOR SP - 223 EP - 231 VL - 28 IS - 2 SN - -2148-9297 M3 - doi: 10.15832/ankutbd.868213 UR - https://doi.org/10.15832/ankutbd.868213 Y2 - 2021 ER -
EndNote %0 Journal of Agricultural Sciences Screening of Antibiotic Resistance and Virulence Genes of Enterococcus spp. Strains Isolated from Urfa Cheese %A Sine Özmen Toğay , Şeniz Karayiğit %T Screening of Antibiotic Resistance and Virulence Genes of Enterococcus spp. Strains Isolated from Urfa Cheese %D 2022 %J Journal of Agricultural Sciences %P -2148-9297 %V 28 %N 2 %R doi: 10.15832/ankutbd.868213 %U 10.15832/ankutbd.868213
ISNAD Özmen Toğay, Sine , Karayiğit, Şeniz . "Screening of Antibiotic Resistance and Virulence Genes of Enterococcus spp. Strains Isolated from Urfa Cheese". Journal of Agricultural Sciences 28 / 2 (April 2022): 223-231 . https://doi.org/10.15832/ankutbd.868213
AMA Özmen Toğay S. , Karayiğit Ş. Screening of Antibiotic Resistance and Virulence Genes of Enterococcus spp. Strains Isolated from Urfa Cheese. J Agr Sci-Tarim Bili. 2022; 28(2): 223-231.
Vancouver Özmen Toğay S. , Karayiğit Ş. Screening of Antibiotic Resistance and Virulence Genes of Enterococcus spp. Strains Isolated from Urfa Cheese. Journal of Agricultural Sciences. 2022; 28(2): 223-231.
IEEE S. Özmen Toğay and Ş. Karayiğit , "Screening of Antibiotic Resistance and Virulence Genes of Enterococcus spp. Strains Isolated from Urfa Cheese", Journal of Agricultural Sciences, vol. 28, no. 2, pp. 223-231, Apr. 2022, doi:10.15832/ankutbd.868213