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Tavuk ve martı kökenli enterokok türlerinin antibiyotik dirençliliğinin fenotipik ve genotipik analizi

Yıl 2016, Cilt: 63 Sayı: 3, 235 - 244, 01.09.2016

Ömer Akgül Timur Gülhan Hüseyin Güdücüoğlu

Öz

Bu çalışmada, Van ili ve ilçelerinde halk elinde yetiştiriciliği yapılan tavuklardan ve Van Gölü Havzasının değişik noktalarında insanlarla ilişki halinde olan martı popülasyonlarından alınan dışkı örnekleri enterokok türleri açısından incelendi. Bu amaçla 500 tavuk ve 500 martı olmak üzere toplam 1000 adet dışkı örneği toplandı. Tavuk dışkı örneklerinden 192 (%38.4) ve martı dışkı örneklerinden ise 119 (%23.8) olmak üzere toplam 311 (%31.1) adet enterokok izole edildi. Tavuk orijinli izolatların 41 (%21.3)’i Enterococcus faecalis, 110 (%57.3)’u E. faecium, 9 (%4.7)’u E. casseliflavus/gallinarum, 27 (%14.1)’si E. hirae, 5 (%2.6)’i E. durans olarak identifiye edilirken; martı orijinlilerin 78 (%65.5)’i E. faecalis, 21 (%17.6)’i E. faecium, 10 (%8.4)’u E. hirae, 7 (%5.9)’si E. casseliflavus/gallinarum, 2 (%1.7)’si E. raffinosus, 1 (%0.8)’i E. durans olarak tanımlandı. Fenotipik analiz, antibiyogram testi (disk difüzyon yöntemi) ile yapıldı. Genotipik olarak ise 16S rRNA, 16S ve 23S arası bölgeler, esp, vanA, vanB ve vanC (C-1,C-2, C-3) genleri analiz edildi. Tüm izolatların antibiyotik dirençlilikleri dikkate alındığında, en fazla dirençlilik sefadroksil (%99.5) en az dirençlilik ise imipenem (%0.8) karşı saptandı. İzolatların 9 (%2.9)’u fenotipik olarak vankomisine dirençli bulunurken, 20 (%6.4)’sinde genotipik olarak vankomisin dirençlilik geni (van) belirlendi. Bunlardan 6 E. faecalis (1’i tavuk, 5’i martı orijinli) ve 3 E. faecium (martı orijinli) izolatının vanA, 6 E. casseliflavus/gallinarium izolatının vanC1 (2’si tavuk, 4’ü martı orijinli) ve 5 E. casseliflavus/gallinarium (tavuk orijinli) izolatının ise vanC2/3 geni taşıdığı tespit edildi. Martı izolatlarında vanC2/3 genlerine raslanılamazken, tavuk ve martı orijinli tüm izolatlar vanB geni açısından negatif bulundu. Sonuç olarak, bu araştırma ile bölgemizde ilk kez vankomisin dirençli enterokok türlerinin varlığı ortaya konuldu

Anahtar Kelimeler

Antibiyogram enterokok martı tavuk VRE

Kaynakça

  • Aarestrup FM, Agerso Y, Gerner–Smidt P, et al. (2000): Comparison of antimicrobial resistance phenoty- pes and resistance genes in Enterococcus faecalis and Ente- rococcus faecium from humans in the community, broylers, and pigs in Denmark. Diag Micro Infect Dis, 37, 127-137.
  • Alp Ş, Şardan YÇ (2008): Vankomisine dirençli entero- kokların epidemiyolojisi ve kontrolü. Hacettepe Med J, 39, 89-95.
  • Boyd DA, Willey BM, Fawcett D, et al. (2008): Molecular characterization of Enterococcus faecalis N06-0364 with low-level vancomycin resistance harboring a novel D-Ala- D-Ser gene cluster, vanL. Antimicrob Agent Chemoter, 52, 2667-2672.
  • Brisse S, Fussing V, Ridwan B, et al. (2002): Automated ribotyping of vancomycin-resistant Enterococcus faecium isolates. JCM, 40, 1977-1984.
  • CLSI (2011): Performance Standards for Antimicrobial Susceptibility Testing; Twenty-first edition: Informational Supplement. CLSI document M100-S21. CLSI. Wayne, PA, USA. 6. Courvalin P (2006): Vancomycin resistance in
  • Pheromone-responsive conjugative vancomycin resistance
  • plasmids in Enterococcus faecalis isolates from humans
  • and chicken feces. AEM, 72, 6544-6553.
  • De Leener E, Martel A, De Graef EM, et al. (2005): Molecular analysis of human, porcine, and poultry Enterococcus faecium isolates and their erm (B) genes. AEM, 71, 2766-2770.
  • Deshpande LM, Fritsche TR, Moet GJ, et al. (2007): Antimicrobial resistance and molecular epidemiology of vancomycin-resistant enterococci from North America and Europe: a report from the SENTRY antimicrobial surveillance program. Diag Microb Infect Dis, 58, 163- 170.
  • Dilik Z, İstanbulluoğlu E (2010): Entansif broyler işlet- meleri ile kırsal tavukçuluk işletmelerindeki hayvanlardan izole edilen enterokokların fenotipik ve genotipik özellikle- ri üzerine çalışmalar. Bornova Vet Bil Derg, 32, 37-46.
  • Doğru AK, Gençay YE, Ayaz ND (2010): Comparison of virulence gene profiles of Enterococcus faecium and Enterococcus faecalis chicken neck skin and faeces isolates. Kafkas Univ Vet Fak Derg, 16, 129-133.
  • Fahr AM, Eigner U, Armbrust M, et al. (2003): Two- center collaborative evaluation of the performance of the BD identification and antimicrobial susceptibility testing of Enterococcus spp. and Staphylococcus spp. JCM, 41, 1135-1142. microbiology system for
  • Fortina MG, Ricci G, Mora D, et al. (2004): Molecular analysis of artisanal Italian cheeses reveals Enterococcus italicus sp. nov. IJSEM, 54, 1717-1721.
  • Frye JG, Jackson CR (2013): Genetic mechanisms of antimicrobial resistance identified in Salmonella enterica, Escherichia coli, and Enteroccocus spp. isolated from US food animals. Front Microbiol, 4, 135.
  • Garcia-Migura L, Pleydell E, Barnes S, et al. (2005): Characterization of vancomycin-resistant Enterococcus faecium isolates from and broyler poultry and pig farms in England and Wales. JCM, 43, 3283-3289.
  • Gülhan T, Boynukara B, Durmus A, et al. (2012): Enteric bacteria and some pathogenic properties of Enterococcus Escherichia coli strains isolated from wild ducks and gulls. FEB, 21, 1961-1966. Enterococcus faecium and
  • Hayes JR, English LL, Carter PJ, et al. (2003): Prevalance and antimicrobial resistance of enterococcus species isolated from retail meats. AEM, 69, 7153-7160.
  • Kariyama R, Mitsuhata R, Chow JW, et al. (2000): Simple and reliable Multiplex PCR assay for surveillance isolates of vancomycin-resistant enterococci. JCM, 38, 3092-3095.
  • Kolář M, Pantůček R, Bardoň J, et al. (2002): Occurrence of antibiotic-resistant bacterial strains isolated in poultry. Vet Med Czech, 47, 52-59.
  • Lauderdale TL, Shiau YR, Wang HY, et al. (2007): Effect of banning vancomycin analogue avoparcin on vancomycin‐resistant enterococci in chicken farms in Taiwan. Environ Microbiol, 9, 819-823.
  • Lebreton F, Depardieu F, Bourdon N, et al. (2011): D- Ala-D-Ser VanN-type transferable vancomycin resistance in Enterococcus faecium. Antimicrob Agent Chemoter, 55, 4606-4612.
  • Lim SK, Tanimoto K, Tomita H, et al. (2006):
  • Lukášová J, Šustáčková A (2003): Enterococci and antibiotic resistance. Acta Vet Brno, 72, 315-323.
  • Mac K, Wichmann-Schauer H, Peters J, et al. (2003): Species identification and detection of vancomycin resistance genes in enterococci of animal origin by multiplex PCR. Int J Food Microbiol, 88, 305-309.
  • Manson JM, Smith JMB, Cook GM (2004): Persistence of vancomycin-resistant enterococci in New Zealand broylers after discontinuation of avoparcin use. AEM, 70, 5764-5768.
  • Mansur A, Ay S, Otlu B, et al. (2013): Karbapenem dirençli Pseudomonas aeruginousa izolatlarında metallo beta laktamaz üretiminin araştırılması. J Turgut Ozal Med Cent, 20, 237-242.
  • Nam S, Kim MJ, Park C, et al. (2013): Detection and genotyping of vancomycin-resistant Enterococcus spp. by multiplex polymerase chain reaction in Korean aquatic environmental samples. IJHEH, 216, 421-427.
  • Ongut G, Kilinckaya H, Baysan BO, et al. (2013): Evaluation of Brilliance VRE agar for the detection of vancomycin-resistant specimens. J Med Microbiol, 62, 661-662. in rectal swab
  • Oravcova V, Ghosh A, Zurek L, et al. (2013): Vancomycin-resistant enterococci in rooks (Corvus frugilegus) Microbiol, 15, 548-556. Europe. Environ
  • Patel R, Uhl JR, Kohner P, et al. (1997): Multiplex PCR detection of vanA, vanB, vanC-1, and vanC2/3 genes in enterococci. JCM, 35, 703-707.
  • Poeta P, Costa D, Klibi N, et al. (2006): Phenotypic and genotypic study of gelatinase and β-haemolysis activities in faecal enterococci of poultry in Portugal. J Vet Med, 53, 203-208.
  • Radhouani H, Pinto L, Coelho C, et al. (2010): MLST and a genetic study of antibiotic resistance and virulance factors in vanA-containing Enterococcus from buzzards (Buteo buteo). SFAM, 50, 537-541.
  • Radu S, Toosa H, Rahim RA, et al. (2001): Occurrence of the vanA and vanC2/3 genes in Enterococcus species isolated from poultry sources in Malaysia. Diag Microbiol Infect Dis, 39, 145-153.
  • Santos T, Silva N, Igrejas G, et al. (2013): Dissemination of antibiotic resistant Enterococcus spp. and Escherichia coli from wild birds of Azores Archipelago. Anaerobe, 24, 25-31.
  • Sedgley CM, Molander A, Flannagan SE, et al. (2005): Virulence, phenotype and genotype characteristics of endodontic Enterococcus spp. Oral Microbiol Immunol, 20, 10-19.
  • Song JH, Ko KS, Oh WS, et al. (2006): High frequency of vancomycin-resistant Enterococcus faecium isolates with VanB phenotype and vanA genotype in Korean hospi- tals. Diagn Microbiol Infect Dis, 56, 401-406.
  • Torres C, Escobar S, Portillo A, et al. (2006): Detection of clonally related vanB2- containing Enterococcus 40. Zar JH (1999): Biostatistical Analysis, Fifth Edition, faecium strains in two Spanish hospitals. J Med Microbiol, 55, 1237-1243.
  • Trivedi K, Cupakova S, Karpiskova R (2011): Virulence factors and antibiotic resistance in enterococci isolated from food-stuffs. Veterinarni Medicina, 56, 352-357.
  • Tsikrikonis G, Maniatis AN, Labrou M, et al. (2012): Difference in biofilm formation and virulence factors between clinical and fecal enterococcal isolates of human and animal orgin. Microb Pathog, 52, 336-343.
  • Xu X, Lin D, Yan G, et al. (2010): vanM, a new glyco- peptide resistance gene cluster found in Enterococcus fa- ecium. Antimicrob Agents Chemother, 54, 4643-4647. Prentice Hall, Upper Saddle River, New Jersey, USA. Geliş tarihi: 16.06.2015 / Kabul tarihi: 12.01.2016

Phenotypic and genotypic analysis for antibiotic resistance of Enterococcus species with chicken and gull origin

Yıl 2016, Cilt: 63 Sayı: 3, 235 - 244, 01.09.2016

Ömer Akgül Timur Gülhan Hüseyin Güdücüoğlu

Öz

In this study, faecal samples of backyard chickens in the city of Van and its districts and gulls in contact with humans in Van Lake basin have been obtained and examined for Enterecoccus species. For this purpose, 1000 faecal samples have been obtained as 500 from chickens and 500 from gulls. In the study, Entrerecoccus has been isolated and identified from a total of 311 (31.1%) faecal samples as 192 (38.4%) from chickens and 119 (23.8%) from gulls. 41 (21.3%) of chicken-origin isolates have been identified as Enterococcus faecalis, 110 (57.3%) as E. faecium, 9 (4.7%) as E. casseliflavus/gallinarum, 27 (14.1%) as E. hirae, 5 (2.6%) E. durans while 78 (65.5%) of gull-origin isolates have been identified as E. faecalis, 21 (17.6%) as E. faecium, 10 (8.4%) as E. hirae, 7 (5.9%) as E. casseliflavus/gallinarum, 2 (1.7%) as E. raffinosus and 1 (0.8%) as E. durans. Phenotypically antibiotic susceptibility testing (disc diffusion method) was performed for analysis. Genotypically 16S rRNA, 16S and 23S intergenic transcribed spacer region, esp, vanA, vanB and vanC (C-1, C-2, C-3) was analyzed genes. When antibiotic resistance of whole isolates have been taken into consideration; the highest level of resistance was determined to cefadroxil (99.5%) while the lowest resistance was determined to imipenem (0.8%). While 9 (2.9%) of the isolates have been determined as resistant to vancomycin; genotypically vancomycin resistance gene (van) has been determined 20 (6.4%) of the isolates. 6 of E. faecalis (1 chicken, 5 gull origin) and 3 of E. faecium (gull origin) isolates have been determined as carrying vanA, 6 E. casseliflavus/gallinarum as carrying vanC1 (2 chicken, 4 gull origin) and 5 E. casseliflavus/gallinarium (chicken origin) as carrying vanC2/3 gene. In gull isolates, while vanC2/3 gene was not determined in gull isolates; all chicken and gull origin isolates have been found negative for vanB gene. As a result, for the first time in our region, this research has revealed the presence of vancomycin-resistant Enterococcus species

Anahtar Kelimeler

Antibiogram chicken Enterecoccus gull VRE

Kaynakça

  • Aarestrup FM, Agerso Y, Gerner–Smidt P, et al. (2000): Comparison of antimicrobial resistance phenoty- pes and resistance genes in Enterococcus faecalis and Ente- rococcus faecium from humans in the community, broylers, and pigs in Denmark. Diag Micro Infect Dis, 37, 127-137.
  • Alp Ş, Şardan YÇ (2008): Vankomisine dirençli entero- kokların epidemiyolojisi ve kontrolü. Hacettepe Med J, 39, 89-95.
  • Boyd DA, Willey BM, Fawcett D, et al. (2008): Molecular characterization of Enterococcus faecalis N06-0364 with low-level vancomycin resistance harboring a novel D-Ala- D-Ser gene cluster, vanL. Antimicrob Agent Chemoter, 52, 2667-2672.
  • Brisse S, Fussing V, Ridwan B, et al. (2002): Automated ribotyping of vancomycin-resistant Enterococcus faecium isolates. JCM, 40, 1977-1984.
  • CLSI (2011): Performance Standards for Antimicrobial Susceptibility Testing; Twenty-first edition: Informational Supplement. CLSI document M100-S21. CLSI. Wayne, PA, USA. 6. Courvalin P (2006): Vancomycin resistance in
  • Pheromone-responsive conjugative vancomycin resistance
  • plasmids in Enterococcus faecalis isolates from humans
  • and chicken feces. AEM, 72, 6544-6553.
  • De Leener E, Martel A, De Graef EM, et al. (2005): Molecular analysis of human, porcine, and poultry Enterococcus faecium isolates and their erm (B) genes. AEM, 71, 2766-2770.
  • Deshpande LM, Fritsche TR, Moet GJ, et al. (2007): Antimicrobial resistance and molecular epidemiology of vancomycin-resistant enterococci from North America and Europe: a report from the SENTRY antimicrobial surveillance program. Diag Microb Infect Dis, 58, 163- 170.
  • Dilik Z, İstanbulluoğlu E (2010): Entansif broyler işlet- meleri ile kırsal tavukçuluk işletmelerindeki hayvanlardan izole edilen enterokokların fenotipik ve genotipik özellikle- ri üzerine çalışmalar. Bornova Vet Bil Derg, 32, 37-46.
  • Doğru AK, Gençay YE, Ayaz ND (2010): Comparison of virulence gene profiles of Enterococcus faecium and Enterococcus faecalis chicken neck skin and faeces isolates. Kafkas Univ Vet Fak Derg, 16, 129-133.
  • Fahr AM, Eigner U, Armbrust M, et al. (2003): Two- center collaborative evaluation of the performance of the BD identification and antimicrobial susceptibility testing of Enterococcus spp. and Staphylococcus spp. JCM, 41, 1135-1142. microbiology system for
  • Fortina MG, Ricci G, Mora D, et al. (2004): Molecular analysis of artisanal Italian cheeses reveals Enterococcus italicus sp. nov. IJSEM, 54, 1717-1721.
  • Frye JG, Jackson CR (2013): Genetic mechanisms of antimicrobial resistance identified in Salmonella enterica, Escherichia coli, and Enteroccocus spp. isolated from US food animals. Front Microbiol, 4, 135.
  • Garcia-Migura L, Pleydell E, Barnes S, et al. (2005): Characterization of vancomycin-resistant Enterococcus faecium isolates from and broyler poultry and pig farms in England and Wales. JCM, 43, 3283-3289.
  • Gülhan T, Boynukara B, Durmus A, et al. (2012): Enteric bacteria and some pathogenic properties of Enterococcus Escherichia coli strains isolated from wild ducks and gulls. FEB, 21, 1961-1966. Enterococcus faecium and
  • Hayes JR, English LL, Carter PJ, et al. (2003): Prevalance and antimicrobial resistance of enterococcus species isolated from retail meats. AEM, 69, 7153-7160.
  • Kariyama R, Mitsuhata R, Chow JW, et al. (2000): Simple and reliable Multiplex PCR assay for surveillance isolates of vancomycin-resistant enterococci. JCM, 38, 3092-3095.
  • Kolář M, Pantůček R, Bardoň J, et al. (2002): Occurrence of antibiotic-resistant bacterial strains isolated in poultry. Vet Med Czech, 47, 52-59.
  • Lauderdale TL, Shiau YR, Wang HY, et al. (2007): Effect of banning vancomycin analogue avoparcin on vancomycin‐resistant enterococci in chicken farms in Taiwan. Environ Microbiol, 9, 819-823.
  • Lebreton F, Depardieu F, Bourdon N, et al. (2011): D- Ala-D-Ser VanN-type transferable vancomycin resistance in Enterococcus faecium. Antimicrob Agent Chemoter, 55, 4606-4612.
  • Lim SK, Tanimoto K, Tomita H, et al. (2006):
  • Lukášová J, Šustáčková A (2003): Enterococci and antibiotic resistance. Acta Vet Brno, 72, 315-323.
  • Mac K, Wichmann-Schauer H, Peters J, et al. (2003): Species identification and detection of vancomycin resistance genes in enterococci of animal origin by multiplex PCR. Int J Food Microbiol, 88, 305-309.
  • Manson JM, Smith JMB, Cook GM (2004): Persistence of vancomycin-resistant enterococci in New Zealand broylers after discontinuation of avoparcin use. AEM, 70, 5764-5768.
  • Mansur A, Ay S, Otlu B, et al. (2013): Karbapenem dirençli Pseudomonas aeruginousa izolatlarında metallo beta laktamaz üretiminin araştırılması. J Turgut Ozal Med Cent, 20, 237-242.
  • Nam S, Kim MJ, Park C, et al. (2013): Detection and genotyping of vancomycin-resistant Enterococcus spp. by multiplex polymerase chain reaction in Korean aquatic environmental samples. IJHEH, 216, 421-427.
  • Ongut G, Kilinckaya H, Baysan BO, et al. (2013): Evaluation of Brilliance VRE agar for the detection of vancomycin-resistant specimens. J Med Microbiol, 62, 661-662. in rectal swab
  • Oravcova V, Ghosh A, Zurek L, et al. (2013): Vancomycin-resistant enterococci in rooks (Corvus frugilegus) Microbiol, 15, 548-556. Europe. Environ
  • Patel R, Uhl JR, Kohner P, et al. (1997): Multiplex PCR detection of vanA, vanB, vanC-1, and vanC2/3 genes in enterococci. JCM, 35, 703-707.
  • Poeta P, Costa D, Klibi N, et al. (2006): Phenotypic and genotypic study of gelatinase and β-haemolysis activities in faecal enterococci of poultry in Portugal. J Vet Med, 53, 203-208.
  • Radhouani H, Pinto L, Coelho C, et al. (2010): MLST and a genetic study of antibiotic resistance and virulance factors in vanA-containing Enterococcus from buzzards (Buteo buteo). SFAM, 50, 537-541.
  • Radu S, Toosa H, Rahim RA, et al. (2001): Occurrence of the vanA and vanC2/3 genes in Enterococcus species isolated from poultry sources in Malaysia. Diag Microbiol Infect Dis, 39, 145-153.
  • Santos T, Silva N, Igrejas G, et al. (2013): Dissemination of antibiotic resistant Enterococcus spp. and Escherichia coli from wild birds of Azores Archipelago. Anaerobe, 24, 25-31.
  • Sedgley CM, Molander A, Flannagan SE, et al. (2005): Virulence, phenotype and genotype characteristics of endodontic Enterococcus spp. Oral Microbiol Immunol, 20, 10-19.
  • Song JH, Ko KS, Oh WS, et al. (2006): High frequency of vancomycin-resistant Enterococcus faecium isolates with VanB phenotype and vanA genotype in Korean hospi- tals. Diagn Microbiol Infect Dis, 56, 401-406.
  • Torres C, Escobar S, Portillo A, et al. (2006): Detection of clonally related vanB2- containing Enterococcus 40. Zar JH (1999): Biostatistical Analysis, Fifth Edition, faecium strains in two Spanish hospitals. J Med Microbiol, 55, 1237-1243.
  • Trivedi K, Cupakova S, Karpiskova R (2011): Virulence factors and antibiotic resistance in enterococci isolated from food-stuffs. Veterinarni Medicina, 56, 352-357.
  • Tsikrikonis G, Maniatis AN, Labrou M, et al. (2012): Difference in biofilm formation and virulence factors between clinical and fecal enterococcal isolates of human and animal orgin. Microb Pathog, 52, 336-343.
  • Xu X, Lin D, Yan G, et al. (2010): vanM, a new glyco- peptide resistance gene cluster found in Enterococcus fa- ecium. Antimicrob Agents Chemother, 54, 4643-4647. Prentice Hall, Upper Saddle River, New Jersey, USA. Geliş tarihi: 16.06.2015 / Kabul tarihi: 12.01.2016
Toplam 41 adet kaynakça vardır.

Ayrıntılar

Diğer ID JA93EN94BD
Bölüm Araştırma Makalesi
Yazarlar

Ömer Akgül

Timur Gülhan

Hüseyin Güdücüoğlu

Yayımlanma Tarihi 1 Eylül 2016
Yayımlandığı Sayı Yıl 2016Cilt: 63 Sayı: 3

Kaynak Göster

APA Akgül, Ö., Gülhan, T., & Güdücüoğlu, H. (2016). Phenotypic and genotypic analysis for antibiotic resistance of Enterococcus species with chicken and gull origin. Ankara Üniversitesi Veteriner Fakültesi Dergisi, 63(3), 235-244.
AMA Akgül Ö, Gülhan T, Güdücüoğlu H. Phenotypic and genotypic analysis for antibiotic resistance of Enterococcus species with chicken and gull origin. Ankara Univ Vet Fak Derg. Eylül 2016;63(3):235-244.
Chicago Akgül, Ömer, Timur Gülhan, ve Hüseyin Güdücüoğlu. “Phenotypic and Genotypic Analysis for Antibiotic Resistance of Enterococcus Species With Chicken and Gull Origin”. Ankara Üniversitesi Veteriner Fakültesi Dergisi 63, sy. 3 (Eylül 2016): 235-44.
EndNote Akgül Ö, Gülhan T, Güdücüoğlu H (01 Eylül 2016) Phenotypic and genotypic analysis for antibiotic resistance of Enterococcus species with chicken and gull origin. Ankara Üniversitesi Veteriner Fakültesi Dergisi 63 3 235–244.
IEEE Ö. Akgül, T. Gülhan, ve H. Güdücüoğlu, “Phenotypic and genotypic analysis for antibiotic resistance of Enterococcus species with chicken and gull origin”, Ankara Univ Vet Fak Derg, c. 63, sy. 3, ss. 235–244, 2016.
ISNAD Akgül, Ömer vd. “Phenotypic and Genotypic Analysis for Antibiotic Resistance of Enterococcus Species With Chicken and Gull Origin”. Ankara Üniversitesi Veteriner Fakültesi Dergisi 63/3 (Eylül 2016), 235-244.
JAMA Akgül Ö, Gülhan T, Güdücüoğlu H. Phenotypic and genotypic analysis for antibiotic resistance of Enterococcus species with chicken and gull origin. Ankara Univ Vet Fak Derg. 2016;63:235–244.
MLA Akgül, Ömer vd. “Phenotypic and Genotypic Analysis for Antibiotic Resistance of Enterococcus Species With Chicken and Gull Origin”. Ankara Üniversitesi Veteriner Fakültesi Dergisi, c. 63, sy. 3, 2016, ss. 235-44.
Vancouver Akgül Ö, Gülhan T, Güdücüoğlu H. Phenotypic and genotypic analysis for antibiotic resistance of Enterococcus species with chicken and gull origin. Ankara Univ Vet Fak Derg. 2016;63(3):235-44.