Research Article
BibTex RIS Cite

Biofilm Forming Capacity and Presence of Biofilm-Associated Virulence Genes of Enterococcus faecalis isolates from Slaughterhouse Environments

Year 2023, Volume: 4 Issue: 1, 12 - 17, 30.06.2023
https://doi.org/10.58833/bozokvetsci.1283247

Abstract

This study aims to investigate the presence of biofilm-producing enterococcus and their biofilm-related virulence factor genes in the slaughter line of a class A cattle slaughterhouse in Kayseri. A total of 300 samples (180 carcasses, 102 equipment and surfaces, and 18 samples of slaughterhouse wastewater) were analyzed using conventional methods and PCR. The biofilm-forming abilities of the isolates were determined using congo red agar and microplate testing, and PCR was used to detect biofilm-associated virulence genes (gelE and esp). E. faecalis was isolated from 40 (13.3%) of analyzed samples, of which 35 (87.5%) produced biofilms. The gelE gene was detected in 33 (82.5%) biofilm-positive isolates, from which one (2.5%) contained also esp gene. In conclusion, this study determined the presence of biofilm-positive E. faecalis among the samples taken from a slaughterhouse in Kayseri province, and the relationship between virulence genes and biofilm formation. In conclusion, it is important for food safety to detect biofilm-positive E. faecalis, reflecting the hygienic quality of the slaughterhouse, in all sample types taken from the slaughterhouse in Kayseri, determining the relationship between the biofilm formation of isolates and virulence factor genes.

References

  • 1. Golob M, Pate M, Kušar D, Dermota U, Avberšek J, Papić B, et al. Antimicrobial Resistance and Virulence Genes in Enterococcus faecium and Enterococcus faecalis from Humans and Retail Red Meat. Biomed Res Int 2019; 2019: 1–12. doi:10.1155/2019/2815279.
  • 2. Cattoir V. The multifaceted lifestyle of enterococci: genetic diversity, ecology and risks for public health. Curr Opin Microbiol 2022; 65: 73–80. doi:10.1016/j.mib.2021.10.013.
  • 3. Azimi Mahalleh A, Göncüoğlu M. Enterokokların önemli virülens faktörleri ve gıdalarda bulunuşu. Etlik Vet Mikrobiyol Derg 2014; 25: 47–52.
  • 4. Ben Braïek O, Smaoui S. Enterococci: Between Emerging Pathogens and Potential Probiotics. Biomed Res Int 2019; 2019: 5938210. doi:10.1155/2019/5938210.
  • 5. Makarov DA, Ivanova OE, Pomazkova A V., Egoreva MA, Prasolova O V., Lenev S V., et al. Antimicrobial resistance of commensal Enterococcus faecalis and Enterococcus faecium from food-producing animals in Russia. Vet World 2022; 15: 611. doi:10.14202/VETWORLD.2022.611-621.
  • 6. Hashem YA, Abdelrahman KA, Aziz RK. Phenotype–genotype correlations and distribution of key virulence factors in Enterococcus faecalis isolated from patients with urinary tract infections. Infect Drug Resist 2021; 14: 1713–23. doi:10.2147/IDR.S305167.
  • 7. Li Y, Pan J, Wu D, Tian Y, Zhang J, Fang J. Regulation of Enterococcus faecalis Biofilm Formation and Quorum Sensing Related Virulence Factors with Ultra-low Dose Reactive Species Produced by Plasma Activated Water. Plasma Chemistry and Plasma Processing 2019; 39: 35–49. doi:10.1007/S11090-018-9930-2.
  • 8. Khalil MA, Alorabi JA, Al-Otaibi LM, Ali SS, Elsilk SE. Antibiotic Resistance and Biofilm Formation in Enterococcus spp. Isolated from Urinary Tract Infections. Pathogens 2022; 12: 34. doi:10.3390/PATHOGENS12010034.
  • 9. Ozkok Z, Bilgin K, Cayci YT, Birinci A. Investigation of biofilm formation of Enterococcus species isolated from blood by phenotypic and genotypic methods. Türk Hijyen ve Deneysel Biyoloji Dergisi 2021; 78: 363–72. doi:10.5505/TurkHijyen.2021.02328.
  • 10. Anderson AC, Jonas D, Huber I, Karygianni L, Wölber J, Hellwig E, et al. Enterococcus faecalis from food, clinical specimens, and oral sites: Prevalence of virulence factors in association with biofilm formation. Front Microbiol 2016; 6: 1534. doi:10.3389/FMICB.2015.01534/BIBTEX.
  • 11. Ramos S, Igrejas G, Capelo-Martinez JL, Poeta P. Antibiotic resistance and mechanisms implicated in fecal enterococci recovered from pigs, cattle and sheep in a Portuguese slaughterhouse. Ann Microbiol 2012; 62: 1485–94. doi:10.1007/S13213-011-0402-7.
  • 12. Wambui J, Tasara T, Njage PMK, Stephan R. Species Distribution and Antimicrobial Profiles of Enterococcus spp. Isolates from Kenyan Small and Medium Enterprise Slaughterhouses. J Food Prot 2018; 81: 1445–9.
  • 13. ISO. Microbiology of the food chain — Carcass sampling for microbiological analysis ISO 17604:2015 -. 2015.
  • 14. Güzel N, Ertaş Onmaz N. Toplu Yemek Üretimi Yapan Bir İşletmede Personel ve Gıda Temas Yüzeylerinin Mikrobiyolojik Yönden Değerlendirilmesi. Journal of The Faculty of Veterinary Medicine Erciyes University 2022; 19: 189–94. doi:10.32707/ERCIVET.1204281.
  • 15. Yoon S, Kim Y Bin, Seo KW, Ha JS, Noh EB, Lee YJ. Characteristics of linezolid-resistant Enterococcus faecalis isolates from broiler breeder farms. Poult Sci 2020; 99: 6055–61. doi:10.1016/J.PSJ.2020.06.087.
  • 16. Sanderson H, Ortega-Polo R, McDermott K, Zaheer R, Brown RS, Majury A, et al. Comparison of biochemical and genotypic speciation methods for vancomycin-resistant enterococci isolated from urban wastewater treatment plants. J Microbiol Methods 2019; 161: 102–10. doi:10.1016/j.mimet.2019.04.019.
  • 17. Delibas Y, Turkyılmaz S. Mastitisli Sığır Süt Örneklerinden Elde Edilen Enterococcus faecium İzolatlarında Bazı Bakteriyosin Genlerinin Saptanması. Van Veterinary Journal 2018; 29: 27–32. doi:10.1186/S13567-017-0425-6.
  • 18. Gajewska J, Chajęcka-Wierzchowska W, Byczkowska-Rostkowska Z, Saki M. Biofilm Formation Capacity and Presence of Virulence Determinants among Enterococcus Species from Milk and Raw Milk Cheeses. Life 2023; 13: 495. doi:10.3390/LIFE13020495/S1.
  • 19. Gürkan T, Külahcı MB, Çıtak S. Gıda örneklerinden izole edilen Enterococcus türlerinin çeşitli virülans özellikleri, biyofilm oluşumu ve antibiyotik dirençliliklerinin belirlenmesi. European Journal of Science and Technology 2021; 28: 924–32. doi:10.31590/ejosat.1012135.
  • 20. Stepanović S, Vuković D, Dakić I, Savić B, Švabić-Vlahović M. A modified microtiter-plate test for quantification of staphylococcal biofilm formation. J Microbiol Methods 2000; 40: 175–9. https://doi.org/10.1016/S0167-7012(00)00122-6.
  • 21. Mete E, Kaleli İ, Cevahir N, Demir M, Akkaya Y, Kiris Satılmıs Ö. Enterokok Türlerinin Virulans Faktörlerinin Araştırılması. Mikrobiyol Bul 2017; 51: 101–14. doi:10.5578/mb.53992.
  • 22. Chingwaru W, Mpuchane SF, Gashe BA. Enterococcus faecalis and Enterococcus faecium Isolates from Milk, Beef, and Chicken and Their Antibiotic Resistance. J Food Prot 2003; 66: 931–6. doi:10.4315/0362-028X-66.6.931.
  • 23. Kim E, Shin SW, Kwak HS, Cha MH, Yang SM, Gwak YS, et al. Prevalence and characteristics of phenicol-oxazolidinone resistance genes in Enterococcus faecalis and Enterococcus faecium isolated from food-producing animals and meat in Korea. Int J Mol Sci 2021; 22: 11335. doi:10.3390/IJMS222111335/S1.
  • 24. Aslam M, Diarra MS, Service C, Rempel H. Characterization of antimicrobial resistance in Enterococcus spp. recovered from a commercial beef processing plant. Foodborne Pathog Dis 2010; 7: 235–41. doi: 10.1089/fpd.2009.0380.
  • 25. Ławniczek-Wałczyk A, Cyprowski M, Górny RL. Distribution of Selected Drug-resistant Enterococcus Species in Meat Plants in Poland. Rocznik Ochrona Środowiska 2022; 24: 345–59. doi:10.54740/ros.2022.024.
  • 26. Schlegelová J, Babák V, Holasová M, Konstantinová L, Necidová L, Šišák F, et al. Microbial contamination after sanitation of food contact surfaces in dairy and meat processing plants. Czech J Food Sci 2010; 28: 450–61. doi:10.17221/65/2009-CJFS.
  • 27. Mansour AM, Nossair MA-S, Soliman FS, Rabah I, Saleh NA. Detection of Enterococcus faecalis as an Indicator Organism in Abattoirs´ Environment as well as Meat. Matrouh Journal of Veterinary Medicine 2023; 3: 12–8.
  • 28. Klein G, Pack A, Reuter G. Antibiotic resistance patterns of enterococci and occurrence of vancomycin-resistant enterococci in raw minced beef and pork in Germany. Appl Environ Microbiol 1998; 64: 1825–30. doi:10.1128/AEM.64.5.18251830.1998/FORMAT/EPUB.
  • 29. Telli N, Telli AE, Biçer Y, Turkal G, Uçar G. Isolation and antimicrobial resistance of vancomycin resistant Enterococcus spp. (VRE) and methicillin-resistant S. aureus (MRSA) on beef and chicken meat, and workers hands from slaughterhouses and retail shops in Turkey. Journal of the Hellenic Veterinary Medical Society 2022; 72: 3345–54. doi:10.12681/jhvms.29373.
  • 30. Gonulalan Z, Bacak M, Ertas N. Evaluation Of Microbiological Indicators For Haccp Cattle Slaughterhouse Line In A Business Operator. MANAS Journal of Engineering 2014; 2: 23–9.
  • 31. Geçer A, Ertaş Onmaz N. Kanatlı Kesimi Aşamalarında E. Coli O157:H7 Varlığının IMS-PZR Yöntemleri ile İncelenmesi. Atatürk Üniversitesi Veteriner Bilimleri Dergisi 2018; 13: 285–92. doi:10.17094/ATAUNIVBD.356910.
  • 32. Igbinosa IH, Raje OC. Characterization of Enterococcus species isolated from abattoir environment in Benin city, Nigeria. Ife Journal of Science 2020; 21: 81. doi:10.4314/IJS.V21I3.8.
  • 33. Igbinosa EO, Beshiru A, Odjadjare EEO. Diversity, antimicrobial characterization and biofilm formation of Enterococci isolated from aquaculture and slaughterhouse sources in Benin City, Nigeria. Ife Journal of Science 2021; 22: 51–63. doi:10.4314/ijs.v22i3.4.
  • 34. Getachew Y, Hassan L, Zakaria Z, Zaid CZM, Yardi A, Shukor RA, et al. Characterization and risk factors of vancomycin-resistant Enterococci (VRE) among animal-affiliated workers in Malaysia. J Appl Microbiol 2012; 113: 1184–95. doi:10.1111/J.1365-2672.2012.05406.X.
  • 35. Usui M, Ozawa S, Onozato H, Kuge R, Obata Y, Uemae T, et al. Antimicrobial susceptibility of indicator bacteria isolated from chickens in Southeast Asian countries (Vietnam, Indonesia and Thailand). J Vet Med Sci 2014; 76: 685–92. doi:10.1292/JVMS.13-0423.
  • 36. Azizi M, Hasanvand B, Kashef M, Alvandi AH,, Abiri R. Virulence Factor and Biofilm Formation in Clinical Enterococcal Isolates of the West of Iran. Jundishapur J Microbiol 2017; 10: 14379. doi:10.5812/jjm.14379. 37. Woźniak-Biel A, Bugla-Płoskońska G, Burdzy J, Korzekwa K, Ploch S, Wieliczko A. Antimicrobial Resistance and Biofilm Formation in Enterococcus spp. Isolated from Humans and Turkeys in Poland. Microb Drug Resist 2019; 25: 277–86. doi:10.1089/MDR.2018.0221.
  • 38. Ch’ng JH, Chong KKL, Lam LN, Wong JJ, Kline KA. Biofilm-associated infection by enterococci. Nature Reviews Microbiology 2018 17: 82–94.
  • 39. Di Rosa R, Creti R, Venditti M, D’Amelio R, Arciola C, Montanaro L, et al. Relationship between biofilm formation, the enterococcal surface protein (Esp) and gelatinase in clinical isolates of Enterococcus faecalis and Enterococcus faecium. FEMS Microbiol Lett 2006; 256: 145–50. doi:10.1111/J.1574-6968.2006.00112.X.
  • 40. Tsikrikonis G, Maniatis AN, Labrou M, Ntokou E, Michail G, Daponte A, et al. Differences in biofilm formation and virulence factors between clinical and fecal enterococcal isolates of human and animal origin. Microb Pathog 2012; 52: 336–43. doi:10.1016/J.MICPATH.2012.03.003.
  • 41. Soares RO, Fedi AC, Reiter KC, Caierão J, D’Azevedo PA. Correlation between biofilm formation and gelE, esp, and agg genes in Enterococcus spp. clinical isolates. Virulence 2014; 5: 634. doi:10.4161/VIRU.28998.

Mezbaha Ortamından İzole edilen Enterococcus faecalis izolatlarının Biyofilm Oluşturma Kapasitesi ve Biyofilm ile İlişkili Virülans Genlerin Varlığı

Year 2023, Volume: 4 Issue: 1, 12 - 17, 30.06.2023
https://doi.org/10.58833/bozokvetsci.1283247

Abstract

Bu çalışmada, Kayseri ilinde mevcut olan birinci sınıf bir sığır mezbahasında kesim hattı boyunca alınan örneklerde biyofilm oluşturma yeteneğine sahip E. faecalis varlığı ve izolatlar da biyofilm ile ilişkili virülans faktör genlerinin araştırılması amaçlandı. Çalışmada, kesimhaneden alınan toplam 300 adet örnekte (180 karkas, 102 ekipman ve yüzey ve 18 mezbaha atık suyu) etkenin varlığı konvansiyonel yöntem ve PZR ile analiz edildi. İzolatların biyofilm oluşturma yeteneklerini belirlemede Kongo kırmızısı agar ve mikroplaka testi ve biyofilm ile ilişkili virülans genlerinin (gelE ve esp) tespitinde PZR kullanıldı. Analiz edilen 300 örneğin 40’ından (%13.3) E. faecalis izole edildi ve bu izolatların 35 (%87.5) biyofilm oluşturma yeteneğinde idi. Biyofilm pozitif olan izolatların 33’ünde (%82.5) gelE geni belirlendi, ayrıca bu izolatların bir tanesini (% 2.5) esp genini de içeriyordu. Sonuç olarak, Kayseri ilindeki kesimhaneden alınan tüm örnek türlerinde mezbahanın hijyenik kalitesini yansıtan biyofilm oluşturma yeteneğine sahip E. faecalis’in tespit edilmesi ve izolatların biyofilm oluşumunun virülans faktör genler ile ilişkisi tespit edilmesi gıda güvenliği açısından önemlidir.

References

  • 1. Golob M, Pate M, Kušar D, Dermota U, Avberšek J, Papić B, et al. Antimicrobial Resistance and Virulence Genes in Enterococcus faecium and Enterococcus faecalis from Humans and Retail Red Meat. Biomed Res Int 2019; 2019: 1–12. doi:10.1155/2019/2815279.
  • 2. Cattoir V. The multifaceted lifestyle of enterococci: genetic diversity, ecology and risks for public health. Curr Opin Microbiol 2022; 65: 73–80. doi:10.1016/j.mib.2021.10.013.
  • 3. Azimi Mahalleh A, Göncüoğlu M. Enterokokların önemli virülens faktörleri ve gıdalarda bulunuşu. Etlik Vet Mikrobiyol Derg 2014; 25: 47–52.
  • 4. Ben Braïek O, Smaoui S. Enterococci: Between Emerging Pathogens and Potential Probiotics. Biomed Res Int 2019; 2019: 5938210. doi:10.1155/2019/5938210.
  • 5. Makarov DA, Ivanova OE, Pomazkova A V., Egoreva MA, Prasolova O V., Lenev S V., et al. Antimicrobial resistance of commensal Enterococcus faecalis and Enterococcus faecium from food-producing animals in Russia. Vet World 2022; 15: 611. doi:10.14202/VETWORLD.2022.611-621.
  • 6. Hashem YA, Abdelrahman KA, Aziz RK. Phenotype–genotype correlations and distribution of key virulence factors in Enterococcus faecalis isolated from patients with urinary tract infections. Infect Drug Resist 2021; 14: 1713–23. doi:10.2147/IDR.S305167.
  • 7. Li Y, Pan J, Wu D, Tian Y, Zhang J, Fang J. Regulation of Enterococcus faecalis Biofilm Formation and Quorum Sensing Related Virulence Factors with Ultra-low Dose Reactive Species Produced by Plasma Activated Water. Plasma Chemistry and Plasma Processing 2019; 39: 35–49. doi:10.1007/S11090-018-9930-2.
  • 8. Khalil MA, Alorabi JA, Al-Otaibi LM, Ali SS, Elsilk SE. Antibiotic Resistance and Biofilm Formation in Enterococcus spp. Isolated from Urinary Tract Infections. Pathogens 2022; 12: 34. doi:10.3390/PATHOGENS12010034.
  • 9. Ozkok Z, Bilgin K, Cayci YT, Birinci A. Investigation of biofilm formation of Enterococcus species isolated from blood by phenotypic and genotypic methods. Türk Hijyen ve Deneysel Biyoloji Dergisi 2021; 78: 363–72. doi:10.5505/TurkHijyen.2021.02328.
  • 10. Anderson AC, Jonas D, Huber I, Karygianni L, Wölber J, Hellwig E, et al. Enterococcus faecalis from food, clinical specimens, and oral sites: Prevalence of virulence factors in association with biofilm formation. Front Microbiol 2016; 6: 1534. doi:10.3389/FMICB.2015.01534/BIBTEX.
  • 11. Ramos S, Igrejas G, Capelo-Martinez JL, Poeta P. Antibiotic resistance and mechanisms implicated in fecal enterococci recovered from pigs, cattle and sheep in a Portuguese slaughterhouse. Ann Microbiol 2012; 62: 1485–94. doi:10.1007/S13213-011-0402-7.
  • 12. Wambui J, Tasara T, Njage PMK, Stephan R. Species Distribution and Antimicrobial Profiles of Enterococcus spp. Isolates from Kenyan Small and Medium Enterprise Slaughterhouses. J Food Prot 2018; 81: 1445–9.
  • 13. ISO. Microbiology of the food chain — Carcass sampling for microbiological analysis ISO 17604:2015 -. 2015.
  • 14. Güzel N, Ertaş Onmaz N. Toplu Yemek Üretimi Yapan Bir İşletmede Personel ve Gıda Temas Yüzeylerinin Mikrobiyolojik Yönden Değerlendirilmesi. Journal of The Faculty of Veterinary Medicine Erciyes University 2022; 19: 189–94. doi:10.32707/ERCIVET.1204281.
  • 15. Yoon S, Kim Y Bin, Seo KW, Ha JS, Noh EB, Lee YJ. Characteristics of linezolid-resistant Enterococcus faecalis isolates from broiler breeder farms. Poult Sci 2020; 99: 6055–61. doi:10.1016/J.PSJ.2020.06.087.
  • 16. Sanderson H, Ortega-Polo R, McDermott K, Zaheer R, Brown RS, Majury A, et al. Comparison of biochemical and genotypic speciation methods for vancomycin-resistant enterococci isolated from urban wastewater treatment plants. J Microbiol Methods 2019; 161: 102–10. doi:10.1016/j.mimet.2019.04.019.
  • 17. Delibas Y, Turkyılmaz S. Mastitisli Sığır Süt Örneklerinden Elde Edilen Enterococcus faecium İzolatlarında Bazı Bakteriyosin Genlerinin Saptanması. Van Veterinary Journal 2018; 29: 27–32. doi:10.1186/S13567-017-0425-6.
  • 18. Gajewska J, Chajęcka-Wierzchowska W, Byczkowska-Rostkowska Z, Saki M. Biofilm Formation Capacity and Presence of Virulence Determinants among Enterococcus Species from Milk and Raw Milk Cheeses. Life 2023; 13: 495. doi:10.3390/LIFE13020495/S1.
  • 19. Gürkan T, Külahcı MB, Çıtak S. Gıda örneklerinden izole edilen Enterococcus türlerinin çeşitli virülans özellikleri, biyofilm oluşumu ve antibiyotik dirençliliklerinin belirlenmesi. European Journal of Science and Technology 2021; 28: 924–32. doi:10.31590/ejosat.1012135.
  • 20. Stepanović S, Vuković D, Dakić I, Savić B, Švabić-Vlahović M. A modified microtiter-plate test for quantification of staphylococcal biofilm formation. J Microbiol Methods 2000; 40: 175–9. https://doi.org/10.1016/S0167-7012(00)00122-6.
  • 21. Mete E, Kaleli İ, Cevahir N, Demir M, Akkaya Y, Kiris Satılmıs Ö. Enterokok Türlerinin Virulans Faktörlerinin Araştırılması. Mikrobiyol Bul 2017; 51: 101–14. doi:10.5578/mb.53992.
  • 22. Chingwaru W, Mpuchane SF, Gashe BA. Enterococcus faecalis and Enterococcus faecium Isolates from Milk, Beef, and Chicken and Their Antibiotic Resistance. J Food Prot 2003; 66: 931–6. doi:10.4315/0362-028X-66.6.931.
  • 23. Kim E, Shin SW, Kwak HS, Cha MH, Yang SM, Gwak YS, et al. Prevalence and characteristics of phenicol-oxazolidinone resistance genes in Enterococcus faecalis and Enterococcus faecium isolated from food-producing animals and meat in Korea. Int J Mol Sci 2021; 22: 11335. doi:10.3390/IJMS222111335/S1.
  • 24. Aslam M, Diarra MS, Service C, Rempel H. Characterization of antimicrobial resistance in Enterococcus spp. recovered from a commercial beef processing plant. Foodborne Pathog Dis 2010; 7: 235–41. doi: 10.1089/fpd.2009.0380.
  • 25. Ławniczek-Wałczyk A, Cyprowski M, Górny RL. Distribution of Selected Drug-resistant Enterococcus Species in Meat Plants in Poland. Rocznik Ochrona Środowiska 2022; 24: 345–59. doi:10.54740/ros.2022.024.
  • 26. Schlegelová J, Babák V, Holasová M, Konstantinová L, Necidová L, Šišák F, et al. Microbial contamination after sanitation of food contact surfaces in dairy and meat processing plants. Czech J Food Sci 2010; 28: 450–61. doi:10.17221/65/2009-CJFS.
  • 27. Mansour AM, Nossair MA-S, Soliman FS, Rabah I, Saleh NA. Detection of Enterococcus faecalis as an Indicator Organism in Abattoirs´ Environment as well as Meat. Matrouh Journal of Veterinary Medicine 2023; 3: 12–8.
  • 28. Klein G, Pack A, Reuter G. Antibiotic resistance patterns of enterococci and occurrence of vancomycin-resistant enterococci in raw minced beef and pork in Germany. Appl Environ Microbiol 1998; 64: 1825–30. doi:10.1128/AEM.64.5.18251830.1998/FORMAT/EPUB.
  • 29. Telli N, Telli AE, Biçer Y, Turkal G, Uçar G. Isolation and antimicrobial resistance of vancomycin resistant Enterococcus spp. (VRE) and methicillin-resistant S. aureus (MRSA) on beef and chicken meat, and workers hands from slaughterhouses and retail shops in Turkey. Journal of the Hellenic Veterinary Medical Society 2022; 72: 3345–54. doi:10.12681/jhvms.29373.
  • 30. Gonulalan Z, Bacak M, Ertas N. Evaluation Of Microbiological Indicators For Haccp Cattle Slaughterhouse Line In A Business Operator. MANAS Journal of Engineering 2014; 2: 23–9.
  • 31. Geçer A, Ertaş Onmaz N. Kanatlı Kesimi Aşamalarında E. Coli O157:H7 Varlığının IMS-PZR Yöntemleri ile İncelenmesi. Atatürk Üniversitesi Veteriner Bilimleri Dergisi 2018; 13: 285–92. doi:10.17094/ATAUNIVBD.356910.
  • 32. Igbinosa IH, Raje OC. Characterization of Enterococcus species isolated from abattoir environment in Benin city, Nigeria. Ife Journal of Science 2020; 21: 81. doi:10.4314/IJS.V21I3.8.
  • 33. Igbinosa EO, Beshiru A, Odjadjare EEO. Diversity, antimicrobial characterization and biofilm formation of Enterococci isolated from aquaculture and slaughterhouse sources in Benin City, Nigeria. Ife Journal of Science 2021; 22: 51–63. doi:10.4314/ijs.v22i3.4.
  • 34. Getachew Y, Hassan L, Zakaria Z, Zaid CZM, Yardi A, Shukor RA, et al. Characterization and risk factors of vancomycin-resistant Enterococci (VRE) among animal-affiliated workers in Malaysia. J Appl Microbiol 2012; 113: 1184–95. doi:10.1111/J.1365-2672.2012.05406.X.
  • 35. Usui M, Ozawa S, Onozato H, Kuge R, Obata Y, Uemae T, et al. Antimicrobial susceptibility of indicator bacteria isolated from chickens in Southeast Asian countries (Vietnam, Indonesia and Thailand). J Vet Med Sci 2014; 76: 685–92. doi:10.1292/JVMS.13-0423.
  • 36. Azizi M, Hasanvand B, Kashef M, Alvandi AH,, Abiri R. Virulence Factor and Biofilm Formation in Clinical Enterococcal Isolates of the West of Iran. Jundishapur J Microbiol 2017; 10: 14379. doi:10.5812/jjm.14379. 37. Woźniak-Biel A, Bugla-Płoskońska G, Burdzy J, Korzekwa K, Ploch S, Wieliczko A. Antimicrobial Resistance and Biofilm Formation in Enterococcus spp. Isolated from Humans and Turkeys in Poland. Microb Drug Resist 2019; 25: 277–86. doi:10.1089/MDR.2018.0221.
  • 38. Ch’ng JH, Chong KKL, Lam LN, Wong JJ, Kline KA. Biofilm-associated infection by enterococci. Nature Reviews Microbiology 2018 17: 82–94.
  • 39. Di Rosa R, Creti R, Venditti M, D’Amelio R, Arciola C, Montanaro L, et al. Relationship between biofilm formation, the enterococcal surface protein (Esp) and gelatinase in clinical isolates of Enterococcus faecalis and Enterococcus faecium. FEMS Microbiol Lett 2006; 256: 145–50. doi:10.1111/J.1574-6968.2006.00112.X.
  • 40. Tsikrikonis G, Maniatis AN, Labrou M, Ntokou E, Michail G, Daponte A, et al. Differences in biofilm formation and virulence factors between clinical and fecal enterococcal isolates of human and animal origin. Microb Pathog 2012; 52: 336–43. doi:10.1016/J.MICPATH.2012.03.003.
  • 41. Soares RO, Fedi AC, Reiter KC, Caierão J, D’Azevedo PA. Correlation between biofilm formation and gelE, esp, and agg genes in Enterococcus spp. clinical isolates. Virulence 2014; 5: 634. doi:10.4161/VIRU.28998.
There are 40 citations in total.

Details

Primary Language Turkish
Subjects Veterinary Sciences
Journal Section Research Articles
Authors

Candan Güngör 0000-0002-4321-2770

Dursun Alp Gündoğ 0000-0002-1581-1813

Nurhan Ertaş Onmaz 0000-0002-4679-6548

Publication Date June 30, 2023
Submission Date April 14, 2023
Published in Issue Year 2023 Volume: 4 Issue: 1

Cite

Vancouver Güngör C, Gündoğ DA, Ertaş Onmaz N. Mezbaha Ortamından İzole edilen Enterococcus faecalis izolatlarının Biyofilm Oluşturma Kapasitesi ve Biyofilm ile İlişkili Virülans Genlerin Varlığı. Bozok Vet Sci. 2023;4(1):12-7.