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PEYNİRDEN İZOLE EDİLEN YÜKSEK SEVİYEDE AMİNOGLİKOZİD DİRENÇLİ ENTEROKOKLARDA VİRÜLENS FAKTÖRLERİN FENOTİPİK VE GENOTİPİK YÖNTEMLER İLE ARAŞTIRILMASI

Year 2019, Volume: 44 Issue: 4, 719 - 732, 01.08.2019
https://doi.org/10.15237/gida.GD19075

Abstract

Bu çalışmanın amacı daha önce peynir
örneklerinden izole edilen yüksek-seviyede aminoglikozid dirençli (YSAD) 54
enterokok izolatında virülens faktörlerin fenotipik ve genotipik yöntemler
kullanılarak araştırılmasıdır. YSAD enterokok izolatlarında α-hemolitik (48.15
%), γ-hemolitik (46.30 %), ve β-hemolitik (5.55 %) aktivite fenotipik olarak
belirlendi. Jelatinaz aktivitesi yalnız
E.
faecalis RG22.4, RG26.1 ve RG26.2
suşlarında tespit edildi.
Polimeraz
zincir reaksiyonu (PZR) ile
E. faecium
RS32.2 hariç YSAD enterokok izolatlarında en az bir virülens genin varlığı
belirlendi. YSAD enterokok izolatlarında en sık görülen genlerin
ccf 
(% 88.89), efaAfs (% 85.19), acm (% 77.78), gelE (% 59.2), cpd (%
51.85) ve
espfs (% 50) olduğu tespit edildi. Fenotipik
ve genotipik testler sonucu, 30 YSAD enterokok izolatında
sessiz gelE geni bulundu. Peynirden izole edilen YSAD
enterokok suşlarında yüksek sıklıkla virülens faktör genlerinin tespit edilmesi
tüketici sağlığı için endişe uyandırıcıdır.

Supporting Institution

Süleyman Demirel Üniversitesi

Project Number

5085-YL1-17

Thanks

Bu çalışmayı 5085-YL1-17 nolu proje ile maddi olarak destekleyen Süleyman Demirel Üniversitesi Bilimsel Araştırma Projeleri Yönetim Birimi’ne teşekkür ederiz. Degnide Ephrem Adifon yüksek lisans eğitimi sürecinde maddi olarak Benin Bursları Ulusal Müdürlüğü ve Türkiye Bilimsel ve Teknolojik Araştırma Kurumu (TÜBİTAK) tarafından desteklenmiştir.

References

  • Abouelnaga, M., Lamas, A., Quintela-Baluja, M., Osman, M., Miranda, J.M., Cepeda, A., Franco, C.M. (2016). Evaluation of the extent of spreading of virulence factors and antibiotic resistance in enterococci isolated from fermented and unfermented foods. Ann Microbiol, 66, 577-585.
  • Avcı, M., Özden-Tuncer, B. (2017). Safety evaluation of enterocin producer Enterococcus sp. strains isolated from traditional Turkish cheeses. Pol J Microbiol, 2, 223-233.Barbosa, J., Gibbs, P.A., Teixeira, P. (2010). Virulence factors among enterococci isolated from traditional fermented meat products produced in the north of Portugal. Food Control, 21, 651-656.
  • Ben Belgacem, Z., Abriouel, H., Ben Omar, N., Lucas, R., Martinez-Canamero, M., Galvez, A., Manai, M. (2010). Antimicrobial activity, safety aspects, and some technological properties of bacteriocinogenic Enterococcus faecium from artisanal Tunisian fermented meat. Food Control, 21(4), 462-470.
  • Bismuth, R., Courvalin, P. (2010). Aminoglycosides and Gram-positive bacteria. In Antibiogram, Courvalin, P., Leclercq, R. Rice, L. (eds), ESKA, Portland, Oregon, the USA, pp. 225-242.
  • Camargo, I.L.B.C., Gilmore, M.S., Darini, A.L.C. (2006) Multilocus sequence typing and analysis of putative virulence factors in vancomycinresistant and vancomycin-sensitive Enterococcus faecium isolates from Brazil. Clin Microbiol Infect, 12, 1123–1130
  • Cancilla, M.R., Powell, I.B., Hillier, A.J., Davidson. B.E. (1992). Rapid genomic fingerprinting of Lactococcus lactis strains by arbitrarily primed polymerase chain reaction with 32P and fluorescent labels. Appl Environ Microbiol, 58, 1772-1775.
  • Cariolato, D., Andrighetto, C., Lombardi, A. (2008). Occurrence of virulence factors and antibiotic resistances in Enterococcus faecalis and Enterococcus faecium collected from dairy and human samples in North Italy. Food Control, 19, 886-892.
  • Chajęcka-Wierzchowska, W., Zandernowska, A., Łaniewska-Trokenheim, Ł. (2017). Virulence factors of Enterococcus spp. presented in food. LWT-Food Sci Technol, 75, 670-676.
  • Charyyev Gök, M., Özden Tuncer, B., Akpınar Kankaya, D., Tuncer, Y. (2019). Bacteriocinogenic properti,es and safety evaluation of Enterococcus faecium YT52 isolated from boza, a traditional cereal based fermented beverage. Journal of Consumer Protection and Food Safety, 14(1), 41-53.
  • Choi, J-M., 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.
  • Consentino, S., Podda, G.S., Corda, A., Fadda, M.E., Deplano, M., Pisano, M.B. (2010). Molecular detection of virulence factors and antibiotic resistance in clinical Enterococcus faecalis strains in Sardinia. J Prev Med Hyg, 1, 31-36.
  • De Perio, M.A., Yarnold, P.R., Warren, J., Noskin, G.A. (2006). Risk factors and outcomes associated with non-Enterococcus faecalis, non-Enterococcus faecium enterococcal bacteremia. Infect Control Hosp Epidemiol, 27, 28-33.
  • Demirgül, F., Tuncer, Y. (2017). Detection of antibiotic resistance and resistance genes in enterococci isolated from sucuk, a traditional Turkish dry-fermented sausage. Korean J Food Sci An, 37(5), 670-681.
  • Domingos-Lopes, M.F.P., Stanton, C., Ross, P.R., Dapkevicius, M.L.E., Silva, C.C.G. (2017). Genetic diversity, safety and technological characterization of lactic acid bacteria isolated from artisanal Pico cheese. J Food Microbiol, 63, 178-190
  • Dworkin, M., Briana, K.K., Dunny, G.M. (2006). Pheromone-inducible conjugation in Enterococcus faecalis: a model fort he evolution of biological complexity. Int J Med Microbiol, 296, 141-147.
  • Eaton, T.J., Gasson, M.J. (2001). Molecular screening of Enterococcus virulence determinants and potential for genetic exchange between food and medical isolates. Appl Environ Microbiol, 67, 1628-1635.
  • Edwards, U., Rogall, T., Blocker, H., Emde, M., Bottger, E.C. (1989). Isolation and direct complete nucleotide determination of entire genes. Characterization of a gene coding for 16S ribosomal RNA. Nucleic Acids Res, 17, 7843-7853.
  • Fifadara, N., Radu, S., Hassan, Z., Beuchat, L.R., Rusul, G. (2003). Hemolytic and nonhemolytic vancomycin-resistant Enterococcus faecalis isolated from beef important to Malaysia. J Food Prot, 66(10), 1845-1850.
  • Foulquié Moreno, M.R., Sarantinopoulos, P., Tsakalidou, E., De Vuyst, L. (2006). The role and application of enterococci in food and health. Int J Food Microbiol, 106, 1-24.
  • Franz, C.M.A.P., Muscholl-Silberhorn, A.B., Yousif, N.M.K., Vancanneyt, M., Swings, J., Holzapfel, W.H. (2001). Incidence of virulence factors and antibiotic resistance among enterococci isolated from food. Appl Environ Microbiol, 67, 4385-4389.
  • Gomes, B.C., Esteves, C.T., Palazzo, I.C.V., Darini, A.L., Felis, G.E., Sechi, L.A., Franco, B.D., De Martinis, E.C. (2008). Prevalence and characterization of Enterococcus spp. isolated from Brazilian foods. Food Microbiol, 25, 668-675.Hanchi, H., Mottawea, W., Sebei, K., Hammami, R. (2018). The genus Enterococcus: between probiotic potential and safety concerns-an update. Front Microbiol, 9, 1791.
  • Inoğlu, Z.N., Tuncer, Y. (2013). Safety assessment of Enterococcus faecium and Enterococcus facalis strains isolated from Turkish tulum cheese. J Food Safety, 33, 369-377.
  • Klare, I., Konstabel, C., Badstubner, D., Werner, G., Witte, W. (2003). Occurrence and spread of antibiotic resistances in Enterococcus faecium. Int J Food Microbiol, 88, 269-290.
  • Niu, H., Yu, H., Hu, T., Tian, G., Zhang, L., Guo, X., Hu, H., Wang, Z. (2016). The prevalence of aminoglycoside-modifying enzyme and virulence genes among enterococci with high-level aminoglycoside resistance in Inner Mongolia, China. Braz J Microbiol, 47, 691-696.
  • Ogier, J.C., Seror, P. (2008). Safety assessment of dairy microorganisms: The Enterococcus genus. Int J Food Microbiol, 126, 291-301.
  • Özdemir, R. (2018). Süt ve süt ürünlerinde yüksek seviyede aminoglikozid dirençli Enterococcus spp. yaygınlığı ve aminoglikozid-modifiye edici enzim (AME) genlerinin belirlenmesi. Süleyman Demirel Üniversitesi Fen Bilimleri Enstitüsü Gıda Mühendisliği Anabilim Dalı Yüksek lisans Tezi, Isparta, Türkiye, 105 s.
  • Özden Tuncer, B., Ay, Z., Tuncer, Y. (2013). Occurrence of enterocin genes, virulence factors, and antibiotic resistance 3 bacteriocin-producer Enterococcus faecium strains isolated from Turkish tulum cheese. Turkish J Biol, 37, 443-449.
  • Özmen Toğay, S., Çelebi Keskin, A., Açık, L., 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.
  • Péréz-Pulido, R., Abriouel, H., Ben Omar, N., Lucas, R., Martinez, M., Galvez, A. (2006). Safety and potential risks of enterococci isolated from traditional fermented capers. Food Chem Toxicol, 44, 2070-2077.
  • Reviriego, C., Eaton, T., Martín, R., Jiménez, E., Fernández, L., Gasson, M.J., Rodríguez, J.M. (2005). Screening of virulence determinants of Enterococcus faecium strains isolated from breast milk. J Hum Lact, 21, 131-137.
  • Reyes, K., Zervos, M., John, J. (2017). Enterococcal infections in adults. In: Antimicrobial Drug Resistance. Mayers, D.L., Sobel, J.D., Ouellette, M., Kaye, K.S., Marchaim, D. (eds), Clinical and Epidemiological Aspects, Volume 2, Springer International Publishing, Berlin, pp. 811-818.
  • Saba Çopur Ş., Şahin, F., Göçmen, J.S. (2016). Determination of virulence and multidrug resistance genes with polymerase chain reaction method in vancomycin-sensitive and -resistant enterococci isolated from clinical samples. Turk J Med Sci, 46(3), 877-891.
  • Santos, S.C., Fraqueza, M.J., Elias, M., Barreto, A.S., Semedo-Lemsaddek, T. (2017). Traditional dry smoked fermented meat sausages: characterization of autochthonous enterococci. LWT-Food Sci Technol, 79, 410-415Semedo, T., Santos, M.A., Lopes, M.F.S., Marques, J.J.F., Crespo, M.T.B., Tenreiro, R. (2003). Virulence factors in food, clinical and reference enterococci: a common trait in the genus? Syst Appl Microbiol, 26, 13-22.
  • Singh, K.V., Nallapareddy, S.R., Murray, B.A. (2007). Importance of the ebp (endocarditis-and biofilm-associated pilus) locus in the pathogenesis of Enterococcus faecalis ascending urinary tract infection. J Infect Dis, 195, 1671-1677.
  • Sparo, M., Delpech, G., Garcia Allende, N. (2018). Impact on public health of the spread on high-level resistance to gentamicin and vancomycin in enterococci. Front Microbiol, 9, 3073.
  • Su, Y.A., Sulavik, M.C., He, P., Makinen, K.K., Makinen, P.L., Fiedler, S., Wirth, R., Clewell, D.B. (1991). Nucleotide sequence of the gelatinase gene (gelE) from Enterococcus faecalis subsp. liquefaciens. Infect Immun, 59, 415-420.
  • Trivedi, K., Cupakova, S., Karpiskova, R. (2011). Virulence factors and antibiotic resistance in enterococci isolated from food-stuffs. Vet Med-Czech, 56, 352-357.
  • Vankerckhoven, V., Van Autgaerden, T., Vael, C., Lammens, C., Chapelle, S., Rossi, R., Jabes, D., Goossens, H. (2004). Development of a multiplex PCR for the detection of asa1, gelE, cylA, esp, and hyl genes in enterococci and survey for virulence determinants among European hospital isolates of Enterococcus faecium. J Clin Microbiol, 42(10), 4473-4479.
  • Yogurtcu, N.N., Tuncer, Y. (2013). Antibiotic susceptibility patterns of Enterococcus strains isolated from Turkish tulum cheese. Int J Dairy Technol, 66, 236-242.
  • Yousif, N.M.K., Dawyndt, P, Abriouel, H., Wijaya, A., Schillinger, U., Vancanneyt, M., Swing, J., Dirar, H.A., Holzapfel, W.H., Franz, C.M.A.P. (2005). Molecular characterization, technological properties and safety aspects of enterococci from ‘Hussuw’, an African fermented sorghum product. J Appl Microbiol, 98, 216-228.
  • Yüceer, Ö., Özden Tuncer, B. (2015). Determination of antibiotic resistance and biogenic amine production of lactic acid bacteria isolated from fermented Turkish sausage (sucuk). J Food Safety, 35, 276-285.

INVESTIGATION OF VIRULENCE FACTORS USING PHENOTYPIC AND GENOTYPIC METHODS IN HIGH-LEVEL AMINOGLYCOSIDE RESISTANT ENTEROCOCCI ISOLATED FROM CHEESE

Year 2019, Volume: 44 Issue: 4, 719 - 732, 01.08.2019
https://doi.org/10.15237/gida.GD19075

Abstract

The aim of this study was to investigate the virulence
factors
using phenotypic
and genotypic methods in 54 high-level aminoglycoside resistant (HLAR)
enterococci
previously isolated from
cheese samples. The α-hemolytic
(48.15 %), γ-hemolytic (46.30 %), and β-hemolytic (5.55 %) activities phenotypically were determined in HLAR enterococci. Gelatinase activity was detected in only E. faecalis RG22.4, RG26.1, and RG26.2 strains. At least one virulence factor gene
was determined using polymerase chain reaction (PCR) in HLAR isolates except
E. faecium RS32.2. The most frequently
virulence genes were detected as
ccf  (88.89 %), efaAfs (85.19 %), acm (77.78 %),
gelE
(59.2 %), cpd (51.85
%)
, and espfs
(50 %) in HLAR enterococci isolates. As a result of phenotypic and
genotypic tests, silent
gelE genes
were found in 30 HLAR enterococci isolates.
Detection of high frequency of
virulence factor genes in
HLAR enterococci strains isolated from cheese is worrying for consumer health.

Project Number

5085-YL1-17

References

  • Abouelnaga, M., Lamas, A., Quintela-Baluja, M., Osman, M., Miranda, J.M., Cepeda, A., Franco, C.M. (2016). Evaluation of the extent of spreading of virulence factors and antibiotic resistance in enterococci isolated from fermented and unfermented foods. Ann Microbiol, 66, 577-585.
  • Avcı, M., Özden-Tuncer, B. (2017). Safety evaluation of enterocin producer Enterococcus sp. strains isolated from traditional Turkish cheeses. Pol J Microbiol, 2, 223-233.Barbosa, J., Gibbs, P.A., Teixeira, P. (2010). Virulence factors among enterococci isolated from traditional fermented meat products produced in the north of Portugal. Food Control, 21, 651-656.
  • Ben Belgacem, Z., Abriouel, H., Ben Omar, N., Lucas, R., Martinez-Canamero, M., Galvez, A., Manai, M. (2010). Antimicrobial activity, safety aspects, and some technological properties of bacteriocinogenic Enterococcus faecium from artisanal Tunisian fermented meat. Food Control, 21(4), 462-470.
  • Bismuth, R., Courvalin, P. (2010). Aminoglycosides and Gram-positive bacteria. In Antibiogram, Courvalin, P., Leclercq, R. Rice, L. (eds), ESKA, Portland, Oregon, the USA, pp. 225-242.
  • Camargo, I.L.B.C., Gilmore, M.S., Darini, A.L.C. (2006) Multilocus sequence typing and analysis of putative virulence factors in vancomycinresistant and vancomycin-sensitive Enterococcus faecium isolates from Brazil. Clin Microbiol Infect, 12, 1123–1130
  • Cancilla, M.R., Powell, I.B., Hillier, A.J., Davidson. B.E. (1992). Rapid genomic fingerprinting of Lactococcus lactis strains by arbitrarily primed polymerase chain reaction with 32P and fluorescent labels. Appl Environ Microbiol, 58, 1772-1775.
  • Cariolato, D., Andrighetto, C., Lombardi, A. (2008). Occurrence of virulence factors and antibiotic resistances in Enterococcus faecalis and Enterococcus faecium collected from dairy and human samples in North Italy. Food Control, 19, 886-892.
  • Chajęcka-Wierzchowska, W., Zandernowska, A., Łaniewska-Trokenheim, Ł. (2017). Virulence factors of Enterococcus spp. presented in food. LWT-Food Sci Technol, 75, 670-676.
  • Charyyev Gök, M., Özden Tuncer, B., Akpınar Kankaya, D., Tuncer, Y. (2019). Bacteriocinogenic properti,es and safety evaluation of Enterococcus faecium YT52 isolated from boza, a traditional cereal based fermented beverage. Journal of Consumer Protection and Food Safety, 14(1), 41-53.
  • Choi, J-M., 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.
  • Consentino, S., Podda, G.S., Corda, A., Fadda, M.E., Deplano, M., Pisano, M.B. (2010). Molecular detection of virulence factors and antibiotic resistance in clinical Enterococcus faecalis strains in Sardinia. J Prev Med Hyg, 1, 31-36.
  • De Perio, M.A., Yarnold, P.R., Warren, J., Noskin, G.A. (2006). Risk factors and outcomes associated with non-Enterococcus faecalis, non-Enterococcus faecium enterococcal bacteremia. Infect Control Hosp Epidemiol, 27, 28-33.
  • Demirgül, F., Tuncer, Y. (2017). Detection of antibiotic resistance and resistance genes in enterococci isolated from sucuk, a traditional Turkish dry-fermented sausage. Korean J Food Sci An, 37(5), 670-681.
  • Domingos-Lopes, M.F.P., Stanton, C., Ross, P.R., Dapkevicius, M.L.E., Silva, C.C.G. (2017). Genetic diversity, safety and technological characterization of lactic acid bacteria isolated from artisanal Pico cheese. J Food Microbiol, 63, 178-190
  • Dworkin, M., Briana, K.K., Dunny, G.M. (2006). Pheromone-inducible conjugation in Enterococcus faecalis: a model fort he evolution of biological complexity. Int J Med Microbiol, 296, 141-147.
  • Eaton, T.J., Gasson, M.J. (2001). Molecular screening of Enterococcus virulence determinants and potential for genetic exchange between food and medical isolates. Appl Environ Microbiol, 67, 1628-1635.
  • Edwards, U., Rogall, T., Blocker, H., Emde, M., Bottger, E.C. (1989). Isolation and direct complete nucleotide determination of entire genes. Characterization of a gene coding for 16S ribosomal RNA. Nucleic Acids Res, 17, 7843-7853.
  • Fifadara, N., Radu, S., Hassan, Z., Beuchat, L.R., Rusul, G. (2003). Hemolytic and nonhemolytic vancomycin-resistant Enterococcus faecalis isolated from beef important to Malaysia. J Food Prot, 66(10), 1845-1850.
  • Foulquié Moreno, M.R., Sarantinopoulos, P., Tsakalidou, E., De Vuyst, L. (2006). The role and application of enterococci in food and health. Int J Food Microbiol, 106, 1-24.
  • Franz, C.M.A.P., Muscholl-Silberhorn, A.B., Yousif, N.M.K., Vancanneyt, M., Swings, J., Holzapfel, W.H. (2001). Incidence of virulence factors and antibiotic resistance among enterococci isolated from food. Appl Environ Microbiol, 67, 4385-4389.
  • Gomes, B.C., Esteves, C.T., Palazzo, I.C.V., Darini, A.L., Felis, G.E., Sechi, L.A., Franco, B.D., De Martinis, E.C. (2008). Prevalence and characterization of Enterococcus spp. isolated from Brazilian foods. Food Microbiol, 25, 668-675.Hanchi, H., Mottawea, W., Sebei, K., Hammami, R. (2018). The genus Enterococcus: between probiotic potential and safety concerns-an update. Front Microbiol, 9, 1791.
  • Inoğlu, Z.N., Tuncer, Y. (2013). Safety assessment of Enterococcus faecium and Enterococcus facalis strains isolated from Turkish tulum cheese. J Food Safety, 33, 369-377.
  • Klare, I., Konstabel, C., Badstubner, D., Werner, G., Witte, W. (2003). Occurrence and spread of antibiotic resistances in Enterococcus faecium. Int J Food Microbiol, 88, 269-290.
  • Niu, H., Yu, H., Hu, T., Tian, G., Zhang, L., Guo, X., Hu, H., Wang, Z. (2016). The prevalence of aminoglycoside-modifying enzyme and virulence genes among enterococci with high-level aminoglycoside resistance in Inner Mongolia, China. Braz J Microbiol, 47, 691-696.
  • Ogier, J.C., Seror, P. (2008). Safety assessment of dairy microorganisms: The Enterococcus genus. Int J Food Microbiol, 126, 291-301.
  • Özdemir, R. (2018). Süt ve süt ürünlerinde yüksek seviyede aminoglikozid dirençli Enterococcus spp. yaygınlığı ve aminoglikozid-modifiye edici enzim (AME) genlerinin belirlenmesi. Süleyman Demirel Üniversitesi Fen Bilimleri Enstitüsü Gıda Mühendisliği Anabilim Dalı Yüksek lisans Tezi, Isparta, Türkiye, 105 s.
  • Özden Tuncer, B., Ay, Z., Tuncer, Y. (2013). Occurrence of enterocin genes, virulence factors, and antibiotic resistance 3 bacteriocin-producer Enterococcus faecium strains isolated from Turkish tulum cheese. Turkish J Biol, 37, 443-449.
  • Özmen Toğay, S., Çelebi Keskin, A., Açık, L., 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.
  • Péréz-Pulido, R., Abriouel, H., Ben Omar, N., Lucas, R., Martinez, M., Galvez, A. (2006). Safety and potential risks of enterococci isolated from traditional fermented capers. Food Chem Toxicol, 44, 2070-2077.
  • Reviriego, C., Eaton, T., Martín, R., Jiménez, E., Fernández, L., Gasson, M.J., Rodríguez, J.M. (2005). Screening of virulence determinants of Enterococcus faecium strains isolated from breast milk. J Hum Lact, 21, 131-137.
  • Reyes, K., Zervos, M., John, J. (2017). Enterococcal infections in adults. In: Antimicrobial Drug Resistance. Mayers, D.L., Sobel, J.D., Ouellette, M., Kaye, K.S., Marchaim, D. (eds), Clinical and Epidemiological Aspects, Volume 2, Springer International Publishing, Berlin, pp. 811-818.
  • Saba Çopur Ş., Şahin, F., Göçmen, J.S. (2016). Determination of virulence and multidrug resistance genes with polymerase chain reaction method in vancomycin-sensitive and -resistant enterococci isolated from clinical samples. Turk J Med Sci, 46(3), 877-891.
  • Santos, S.C., Fraqueza, M.J., Elias, M., Barreto, A.S., Semedo-Lemsaddek, T. (2017). Traditional dry smoked fermented meat sausages: characterization of autochthonous enterococci. LWT-Food Sci Technol, 79, 410-415Semedo, T., Santos, M.A., Lopes, M.F.S., Marques, J.J.F., Crespo, M.T.B., Tenreiro, R. (2003). Virulence factors in food, clinical and reference enterococci: a common trait in the genus? Syst Appl Microbiol, 26, 13-22.
  • Singh, K.V., Nallapareddy, S.R., Murray, B.A. (2007). Importance of the ebp (endocarditis-and biofilm-associated pilus) locus in the pathogenesis of Enterococcus faecalis ascending urinary tract infection. J Infect Dis, 195, 1671-1677.
  • Sparo, M., Delpech, G., Garcia Allende, N. (2018). Impact on public health of the spread on high-level resistance to gentamicin and vancomycin in enterococci. Front Microbiol, 9, 3073.
  • Su, Y.A., Sulavik, M.C., He, P., Makinen, K.K., Makinen, P.L., Fiedler, S., Wirth, R., Clewell, D.B. (1991). Nucleotide sequence of the gelatinase gene (gelE) from Enterococcus faecalis subsp. liquefaciens. Infect Immun, 59, 415-420.
  • Trivedi, K., Cupakova, S., Karpiskova, R. (2011). Virulence factors and antibiotic resistance in enterococci isolated from food-stuffs. Vet Med-Czech, 56, 352-357.
  • Vankerckhoven, V., Van Autgaerden, T., Vael, C., Lammens, C., Chapelle, S., Rossi, R., Jabes, D., Goossens, H. (2004). Development of a multiplex PCR for the detection of asa1, gelE, cylA, esp, and hyl genes in enterococci and survey for virulence determinants among European hospital isolates of Enterococcus faecium. J Clin Microbiol, 42(10), 4473-4479.
  • Yogurtcu, N.N., Tuncer, Y. (2013). Antibiotic susceptibility patterns of Enterococcus strains isolated from Turkish tulum cheese. Int J Dairy Technol, 66, 236-242.
  • Yousif, N.M.K., Dawyndt, P, Abriouel, H., Wijaya, A., Schillinger, U., Vancanneyt, M., Swing, J., Dirar, H.A., Holzapfel, W.H., Franz, C.M.A.P. (2005). Molecular characterization, technological properties and safety aspects of enterococci from ‘Hussuw’, an African fermented sorghum product. J Appl Microbiol, 98, 216-228.
  • Yüceer, Ö., Özden Tuncer, B. (2015). Determination of antibiotic resistance and biogenic amine production of lactic acid bacteria isolated from fermented Turkish sausage (sucuk). J Food Safety, 35, 276-285.
There are 41 citations in total.

Details

Primary Language Turkish
Journal Section Articles
Authors

Yasin Tuncer 0000-0002-2075-5027

Degnide Ephrem Adıfon This is me

Project Number 5085-YL1-17
Publication Date August 1, 2019
Published in Issue Year 2019 Volume: 44 Issue: 4

Cite

APA Tuncer, Y., & Adıfon, D. E. (2019). PEYNİRDEN İZOLE EDİLEN YÜKSEK SEVİYEDE AMİNOGLİKOZİD DİRENÇLİ ENTEROKOKLARDA VİRÜLENS FAKTÖRLERİN FENOTİPİK VE GENOTİPİK YÖNTEMLER İLE ARAŞTIRILMASI. Gıda, 44(4), 719-732. https://doi.org/10.15237/gida.GD19075
AMA Tuncer Y, Adıfon DE. PEYNİRDEN İZOLE EDİLEN YÜKSEK SEVİYEDE AMİNOGLİKOZİD DİRENÇLİ ENTEROKOKLARDA VİRÜLENS FAKTÖRLERİN FENOTİPİK VE GENOTİPİK YÖNTEMLER İLE ARAŞTIRILMASI. The Journal of Food. August 2019;44(4):719-732. doi:10.15237/gida.GD19075
Chicago Tuncer, Yasin, and Degnide Ephrem Adıfon. “PEYNİRDEN İZOLE EDİLEN YÜKSEK SEVİYEDE AMİNOGLİKOZİD DİRENÇLİ ENTEROKOKLARDA VİRÜLENS FAKTÖRLERİN FENOTİPİK VE GENOTİPİK YÖNTEMLER İLE ARAŞTIRILMASI”. Gıda 44, no. 4 (August 2019): 719-32. https://doi.org/10.15237/gida.GD19075.
EndNote Tuncer Y, Adıfon DE (August 1, 2019) PEYNİRDEN İZOLE EDİLEN YÜKSEK SEVİYEDE AMİNOGLİKOZİD DİRENÇLİ ENTEROKOKLARDA VİRÜLENS FAKTÖRLERİN FENOTİPİK VE GENOTİPİK YÖNTEMLER İLE ARAŞTIRILMASI. Gıda 44 4 719–732.
IEEE Y. Tuncer and D. E. Adıfon, “PEYNİRDEN İZOLE EDİLEN YÜKSEK SEVİYEDE AMİNOGLİKOZİD DİRENÇLİ ENTEROKOKLARDA VİRÜLENS FAKTÖRLERİN FENOTİPİK VE GENOTİPİK YÖNTEMLER İLE ARAŞTIRILMASI”, The Journal of Food, vol. 44, no. 4, pp. 719–732, 2019, doi: 10.15237/gida.GD19075.
ISNAD Tuncer, Yasin - Adıfon, Degnide Ephrem. “PEYNİRDEN İZOLE EDİLEN YÜKSEK SEVİYEDE AMİNOGLİKOZİD DİRENÇLİ ENTEROKOKLARDA VİRÜLENS FAKTÖRLERİN FENOTİPİK VE GENOTİPİK YÖNTEMLER İLE ARAŞTIRILMASI”. Gıda 44/4 (August 2019), 719-732. https://doi.org/10.15237/gida.GD19075.
JAMA Tuncer Y, Adıfon DE. PEYNİRDEN İZOLE EDİLEN YÜKSEK SEVİYEDE AMİNOGLİKOZİD DİRENÇLİ ENTEROKOKLARDA VİRÜLENS FAKTÖRLERİN FENOTİPİK VE GENOTİPİK YÖNTEMLER İLE ARAŞTIRILMASI. The Journal of Food. 2019;44:719–732.
MLA Tuncer, Yasin and Degnide Ephrem Adıfon. “PEYNİRDEN İZOLE EDİLEN YÜKSEK SEVİYEDE AMİNOGLİKOZİD DİRENÇLİ ENTEROKOKLARDA VİRÜLENS FAKTÖRLERİN FENOTİPİK VE GENOTİPİK YÖNTEMLER İLE ARAŞTIRILMASI”. Gıda, vol. 44, no. 4, 2019, pp. 719-32, doi:10.15237/gida.GD19075.
Vancouver Tuncer Y, Adıfon DE. PEYNİRDEN İZOLE EDİLEN YÜKSEK SEVİYEDE AMİNOGLİKOZİD DİRENÇLİ ENTEROKOKLARDA VİRÜLENS FAKTÖRLERİN FENOTİPİK VE GENOTİPİK YÖNTEMLER İLE ARAŞTIRILMASI. The Journal of Food. 2019;44(4):719-32.

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