Araştırma Makalesi
BibTex RIS Kaynak Göster

ÜROPATOJEN E. COLI (UPEC) SUŞLARINDA SINIF I VE SINIF II İNTEGRONLARIN YÜKSEK PREVALANSI İLE ANTİBİYOTİK DİRENCİ, FİLOGRUP VE VİRULANS İLİŞKİSİ

Yıl 2022, Cilt: 85 Sayı: 1, 77 - 85, 25.01.2022
https://doi.org/10.26650/IUITFD.984487

Öz

Amaç: Gen kasetlerinin yakalanması, integrasyonu ve ekspresyonunda oldukça etkin olan integronlar, çoğul antibiyotik direncinin yayılımında önemli bir rol oynarlar. Bu çalışmada, üropatojen E. coli (UPEC) suşlarında integron varlığının antibiyotik direnci, virülans ve filogenetik gruplar ile ve filogrupların, virulans ve antibiyotik direnci ile ilişkisi araştırılmıştır. Gereç ve Yöntemler: Komplike olmayan sistit ve komplike olmayan piyelonefrit etkeni olarak izole edilen 50 UPEC suşu sınıf I, II ve III integronların varlığı ve filogruplarının belirlenmesi amacıyla PCR yöntemi ile incelenmiştir. Elde edilen sonuçlar istatistiki ilişki açısından daha önceki araştırmamızdan elde ettiğimiz bulgular ile incelenmiştir. Bulgular: Elli UPEC suşunun 37’sinin (%74) sınıf I integron, 22’sinin (%44) sınıf II integron ve bir suşun (%2) ise sınıf III integron taşıdığı belirlenmiştir. Yirmi bir (%42) suşun ise sınıf I ve sınıf II integronları birlikte taşıdığı gösterilmiştir. Suşların çoğu B2 (%38) ve E (%38) filogruplarında sınıflandırılmıştır. İntegronların varlığı ile sadece ampisilin direnci ilişkili bulunmuştur (p=0,014). İntegronların varlığı ile virulans genleri veya filogruplar arasında bir ilişki bulunmamıştır; ancak PAI (p<0,001), ompT (p=0,035) ve usp (p<0,001) genlerinin varlığı ile B2 filogrubu arasında anlamlı ilişkili bulunmuştur. Filogrup E ile ko-trimoksazol direnci arasında anlamlı ilişkili bulunmuştur (p=0,043). Sonuç: Bulgularımız literatürle de uyumlu olarak UPEC suşlarında antibiyotik direnci ile integronların (özellikle sınıf I) varlığı arasında güçlü bir ilişki olduğunu kanıtlamış ve tüm dünya genelinde integronların yaygın görüldüğü anlaşılmıştır.

Destekleyen Kurum

Türkiye Bilimsel ve Teknolojik Araştırma Kurumu (TÜBİTAK)

Proje Numarası

2209-a

Kaynakça

  • 1. Azam H, Ghezeljeh SM, Mahmoud S. Prevalence of class 1 and 2 integrons among the multidrug resistant uropathogenic strains of Escherichia coli. Asian Biomed 2017;9(1):49-54. [CrossRef]
  • 2. Ebrahim-Saraie HS, Nezhad NZ, Heidari H, Motamedifar A, Motamedifar M. Detection of antimicrobial susceptibility and integrons among extended-spectrum ß-lactamase producing uropathogenic Escherichia coli isolates in Southwestern Iran. Oman Medical J 2018;33(3):218-23. [CrossRef]
  • 3. Yekani M, Memar MY, Baghi HB, Sefidan FY, Alizadeh N, Ghotaslou R. Association of integrons with multidrugresistant isolates among phylogenic groups of uropathogenic Escherichia coli. Microbiol Res 2018;9(1):10- 3. [CrossRef]
  • 4. El-Najjar N, Farah MJ, Hashwa FA, Tokajian ST. Antibiotic resistance patterns and sequencing of class I integron from uropathogenic Escherichia coli in Lebanon. Lett App Microbiol 2010;51(4):456-61. [CrossRef]
  • 5. Khoramrooz SS, Sharifi A, Yazdanpanah M, Hosseini SAAM, Emaneini M, Gharibpour F et al. High frequency of class 1 integrons in Escherichia coli isolated from patients with urinary tract infections in Yasuj, Iran. Iranian Red Crescent Med Journal 2016;18(1):1-6. [CrossRef]
  • 6. Poey ME, Laviña M. Integrons in uropathogenic Escherichia coli and their relationship with phylogeny and virulence. Microbiol Patho 2014;77:73-7. [CrossRef]
  • 7. Ochoa SA, Cruz-Córdova A, Luna-Pineda VM, Reyes- Grajeda JP, Cázares-Domínguez V, Escalona G, et al. Multidrug-and extensively drug-resistant uropathogenic Escherichia coli clinical strains: phylogenetic groups widely associated with integrons maintain high genetic diversity. Front in Microbiol 2016;7(2042):1-12. [CrossRef]
  • 8. Partridge SR, Tsafnat G, Coiera E, Iredell JR. Gene cassettes and cassette arrays in mobile resistance integrons. FEMS Microbiol Rev 2009;33(4):757-84. [CrossRef]
  • 9. Oliveira-Pinto C, Diamantino C, Oliveira PL, Reis MP, Costa PS, Paiva MC et al. Occurrence and characterization of class 1 integrons in Escherichia coli from healthy individuals and those with urinary infection. J Med Microbiol 2017;66(5):577- 83. [CrossRef]
  • 10. Falakian Z, Nikokar I, Nafisi MR, Karimi A, Validi M. Frequency of class 1 integrons among Escherichia coli isolates of patients with urinary tract infection. Arch of Clin Infect Dis 2012;6(4):1-4.
  • 11. Mandal P, Kapil A, Goswami K, Das B, Dwivedi SN. Uropathogenic Escherichia coli causing urinary tract infections. Indian J Med Res 2001;114:207-11.
  • 12. Puente JL, Brettfinlay B. Pathogenic E. coli. In Groisman EA (ed) Principles of Bacterial Pathogenesis. California: Academic Press, 2001;388-428.
  • 13. Yamamoto S. Molecular epidemiology of uropathogenic Escherichia coli. J Infect Chemother 2007;13:68-73. [CrossRef]
  • 14. Miyazaki J, Ba-Thein W, Kumao T, Obata Yasuoka M, Akaza H, Hayshi H. Type 1, P and S fimbriae, and afimbrial adhesin I are not essential for uropathogenic Escherichia coli to adhere to and invade bladder epithelial cells. FEMS Immunol Med Microbiol 2002;25:23-6. [CrossRef]
  • 15. Uzun C, Oncül O, Gümüş D, Alan S, Dayioğlu N, Küçüker MA. Virulence genes and antibiotic susceptibilities of uropathogenic E. coli strains. Clin Lab 2015;61(8):941-50. [CrossRef]
  • 16. Nougayrède JP, Fernandes PJ, Donnenberg MS. Adhesion of enteropathogenic Escherichia coli to host cells. Cell Microbiol 2003;5:359-72. [CrossRef]
  • 17. Clermont O, Bonacorsi S, Bingen E. Rapid and simple determination of the Escherichia coli phylogenetic group. Applied Environ Microbiol 2000;66(10):4555-8. [CrossRef]
  • 18. Clermont O, Christenson JK, Denamur E, Gordon DM. The Clermont Escherichia coli phylo-typing method revisited: improvement of specificity and detection of new phylo-groups. Environ Microbiol Reports 2013;5(1):58-65. [CrossRef]
  • 19. Khairy RM, Mohamed ES, Abdel Ghany HM, Abdelrahim SS. Phylogenic classification and virulence genes profiles of uropathogenic E. coli and diarrheagenic E. coli strains isolated from community acquired infections. PLoS One 2019;14(9):1-10. [CrossRef]
  • 20. Ren C, Zhao Y, Shen Y. Analysis of the effect of integrons on drug-resistant Staphylococcus aureus by multiplex PCR detection. Molecular Med Reports 2013;7(3):719-24. [CrossRef]
  • 21. Goldstein C, Lee MD, Sanchez S, Hudson C, Phillips B, Register B, et al. Incidence of class 1 and 2 integrases in clinical and commensal bacteria from livestock, companion animals, and exotics. Antimicrob Agents Chemother 2001;45(3):723-6. [CrossRef]
  • 22. Farshad S, Japoni A, Hosseini M. Low distribution of integrons among multidrug resistant E. coli strains isolated from children with community-acquired urinary tract infections in Shiraz, Iran. Pol J Microbiol 2008;57(3):193-8.
  • 23. Mirnezami M, Ranjbar R, Niakan M, Ahmadi MH. Frequency of antimicrobial resistance and class 1 and 2 integrons in Escherichia coli strains isolated from urinary tract infections. Iran J Pharma Res 2020;19(3):282-7.
  • 24. Al-Assil B, Mahfoud M, Hamzeh AR. First report on class 1 integrons and Trimethoprim-resistance genes from dfrA group in uropathogenic E. coli (UPEC) from the Aleppo area in Syria. Mob Gen Elements 2013;3(3):1-6. [CrossRef]
  • 25. Solberg OD, Ajiboye RM, Riley LW. Origin of class 1 and 2 integrons and gene cassettes in a population-based sample of uropathogenic Escherichia coli. J Clin Microbiol 2006;44(4):1347-51. [CrossRef]
  • 26. Zeighami H, Haghi F, Masumian N, Hemmati F, Samei A, Naderi G. Distribution of integrons and gene cassettes among uropathogenic and diarrheagenic Escherichia coli isolates in Iran. Microb Drug Resist 2015;21(4):435-40. [CrossRef]
  • 27. Halaji M, Feizi A, Mirzaei A, Sedigh Ebrahim-Saraie H, Fayyazi A, Ashraf A, et al. The Global Prevalence of Class 1 Integron and associated antibiotic resistance in Escherichia coli from patients with urinary tract infections, a systematic review and Meta-Analysis. Microb Drug Resist 2020;26(10):1208-18. [CrossRef]
  • 28. Çopur ÇA, Sandallı C, Budak EE, Yağmur G, Cizmeci Z, Ak S, et al. Characterization of class 1 and class 2 integron gene cassettes in Escherichia coli strains isolated from urine cultures: a multicenter study. Mikrobiyol Bult 2016;50(2):175- 85. [CrossRef]
  • 29. Gündoğdu A, Long YB, Vollmerhausen TL, Katouli M. Antimicrobial resistance and distribution of sul genes and integron-associated intI genes among uropathogenic Escherichia coli in Queensland, Australia. J Med Microbiol 2011;60(11):1633-42. [CrossRef]
  • 30. Düzgün AÖ, Okumuş F, Saral A, Çiçek AÇ, Cinemre S. Determination of antibiotic resistance genes and virulence factors in Escherichia coli isolated from Turkish patients with urinary tract infection. Revista da Sociedade Brasileira de Medi Tropic 2019;52:1-5. [CrossRef]
  • 31. Lee JH, Subhadra B, Son YJ, Kim DH, Park HS, Kim JM, et al. Phylogenetic group distributions, virulence factors and antimicrobial resistance properties of uropathogenic Escherichia coli strains isolated from patients with urinary tract infections in South Korea. Lett App Microbiol 2016;62(1):84-90. [CrossRef]
  • 32. Yılmaz EŞ, Aslantaş Ö. Phylogenetic group/subgroups distributions, virulence factors, and antimicrobial susceptibility of Escherichia coli strains from urinary tract infections in Hatay. Revista da Sociedade Brasileira de Medi Tropic 2020;53:1-6. [CrossRef]

HIGH PREVALENCE OF CLASS I AND CLASS II INTEGRONS IN UROPATHOGENIC E. COLI STRAINS (UPECs) AND THEIR RELATIONSHIP WITH ANTIBIOTIC RESISTANCE, PHYLOGENY AND VIRULENCE

Yıl 2022, Cilt: 85 Sayı: 1, 77 - 85, 25.01.2022
https://doi.org/10.26650/IUITFD.984487

Öz

Objective: Integrons, which are highly effective in capturing, integrating and expressing gene cassettes, play an important role in the dissemination of multiple antibiotic resistances. This study investigated the correlations of integrons in uropathogenic E. coli (UPEC) with antibiotic resistance, virulence and phylogeny and also the relationships of phylogroups with virulence and antibiotic resistance. Material and Methods: Fifty UPECs isolated from uncomplicated cystitis and uncomplicated pyelonephritis were investigated to detect the presence of class I, II and III integrons and phylogenetic grouping by the PCR method. Their statistical relationship with antibiotic resistance and virulence genes were investigated using our previous findings. Results: Among 50 UPEC strains, 37 (74%), 22 (44%) and only one (2%) strain was shown to harbor class I, class II and class III integrons, respectively. Twenty one (42%) strains were found to carry both class I and class II integrons. The majority of the strains were grouped as phylogroup B2 (38%) and phylogroup E (38%). The presence of integrons was in association with only ampicillin resistance (p=0.014). Integrons was found to be related neither to virulence genes nor phylogroups; however, the presence of PAI (p<0.001), ompT (p=0.035), and usp (p<0.001) genes was foundto be significantly related to phylogroup B2. Phylogroup E was found to be statistically significantly correlated with co-trimoxazole resistance (p=0.043). Conclusion: Consistent with previous studies, our results have proven that there is a strong association between antibiotic resistance and the presence of integrons (especially class I) in UPEC strains, and it has been shown that integrons became very prevalent globally.

Proje Numarası

2209-a

Kaynakça

  • 1. Azam H, Ghezeljeh SM, Mahmoud S. Prevalence of class 1 and 2 integrons among the multidrug resistant uropathogenic strains of Escherichia coli. Asian Biomed 2017;9(1):49-54. [CrossRef]
  • 2. Ebrahim-Saraie HS, Nezhad NZ, Heidari H, Motamedifar A, Motamedifar M. Detection of antimicrobial susceptibility and integrons among extended-spectrum ß-lactamase producing uropathogenic Escherichia coli isolates in Southwestern Iran. Oman Medical J 2018;33(3):218-23. [CrossRef]
  • 3. Yekani M, Memar MY, Baghi HB, Sefidan FY, Alizadeh N, Ghotaslou R. Association of integrons with multidrugresistant isolates among phylogenic groups of uropathogenic Escherichia coli. Microbiol Res 2018;9(1):10- 3. [CrossRef]
  • 4. El-Najjar N, Farah MJ, Hashwa FA, Tokajian ST. Antibiotic resistance patterns and sequencing of class I integron from uropathogenic Escherichia coli in Lebanon. Lett App Microbiol 2010;51(4):456-61. [CrossRef]
  • 5. Khoramrooz SS, Sharifi A, Yazdanpanah M, Hosseini SAAM, Emaneini M, Gharibpour F et al. High frequency of class 1 integrons in Escherichia coli isolated from patients with urinary tract infections in Yasuj, Iran. Iranian Red Crescent Med Journal 2016;18(1):1-6. [CrossRef]
  • 6. Poey ME, Laviña M. Integrons in uropathogenic Escherichia coli and their relationship with phylogeny and virulence. Microbiol Patho 2014;77:73-7. [CrossRef]
  • 7. Ochoa SA, Cruz-Córdova A, Luna-Pineda VM, Reyes- Grajeda JP, Cázares-Domínguez V, Escalona G, et al. Multidrug-and extensively drug-resistant uropathogenic Escherichia coli clinical strains: phylogenetic groups widely associated with integrons maintain high genetic diversity. Front in Microbiol 2016;7(2042):1-12. [CrossRef]
  • 8. Partridge SR, Tsafnat G, Coiera E, Iredell JR. Gene cassettes and cassette arrays in mobile resistance integrons. FEMS Microbiol Rev 2009;33(4):757-84. [CrossRef]
  • 9. Oliveira-Pinto C, Diamantino C, Oliveira PL, Reis MP, Costa PS, Paiva MC et al. Occurrence and characterization of class 1 integrons in Escherichia coli from healthy individuals and those with urinary infection. J Med Microbiol 2017;66(5):577- 83. [CrossRef]
  • 10. Falakian Z, Nikokar I, Nafisi MR, Karimi A, Validi M. Frequency of class 1 integrons among Escherichia coli isolates of patients with urinary tract infection. Arch of Clin Infect Dis 2012;6(4):1-4.
  • 11. Mandal P, Kapil A, Goswami K, Das B, Dwivedi SN. Uropathogenic Escherichia coli causing urinary tract infections. Indian J Med Res 2001;114:207-11.
  • 12. Puente JL, Brettfinlay B. Pathogenic E. coli. In Groisman EA (ed) Principles of Bacterial Pathogenesis. California: Academic Press, 2001;388-428.
  • 13. Yamamoto S. Molecular epidemiology of uropathogenic Escherichia coli. J Infect Chemother 2007;13:68-73. [CrossRef]
  • 14. Miyazaki J, Ba-Thein W, Kumao T, Obata Yasuoka M, Akaza H, Hayshi H. Type 1, P and S fimbriae, and afimbrial adhesin I are not essential for uropathogenic Escherichia coli to adhere to and invade bladder epithelial cells. FEMS Immunol Med Microbiol 2002;25:23-6. [CrossRef]
  • 15. Uzun C, Oncül O, Gümüş D, Alan S, Dayioğlu N, Küçüker MA. Virulence genes and antibiotic susceptibilities of uropathogenic E. coli strains. Clin Lab 2015;61(8):941-50. [CrossRef]
  • 16. Nougayrède JP, Fernandes PJ, Donnenberg MS. Adhesion of enteropathogenic Escherichia coli to host cells. Cell Microbiol 2003;5:359-72. [CrossRef]
  • 17. Clermont O, Bonacorsi S, Bingen E. Rapid and simple determination of the Escherichia coli phylogenetic group. Applied Environ Microbiol 2000;66(10):4555-8. [CrossRef]
  • 18. Clermont O, Christenson JK, Denamur E, Gordon DM. The Clermont Escherichia coli phylo-typing method revisited: improvement of specificity and detection of new phylo-groups. Environ Microbiol Reports 2013;5(1):58-65. [CrossRef]
  • 19. Khairy RM, Mohamed ES, Abdel Ghany HM, Abdelrahim SS. Phylogenic classification and virulence genes profiles of uropathogenic E. coli and diarrheagenic E. coli strains isolated from community acquired infections. PLoS One 2019;14(9):1-10. [CrossRef]
  • 20. Ren C, Zhao Y, Shen Y. Analysis of the effect of integrons on drug-resistant Staphylococcus aureus by multiplex PCR detection. Molecular Med Reports 2013;7(3):719-24. [CrossRef]
  • 21. Goldstein C, Lee MD, Sanchez S, Hudson C, Phillips B, Register B, et al. Incidence of class 1 and 2 integrases in clinical and commensal bacteria from livestock, companion animals, and exotics. Antimicrob Agents Chemother 2001;45(3):723-6. [CrossRef]
  • 22. Farshad S, Japoni A, Hosseini M. Low distribution of integrons among multidrug resistant E. coli strains isolated from children with community-acquired urinary tract infections in Shiraz, Iran. Pol J Microbiol 2008;57(3):193-8.
  • 23. Mirnezami M, Ranjbar R, Niakan M, Ahmadi MH. Frequency of antimicrobial resistance and class 1 and 2 integrons in Escherichia coli strains isolated from urinary tract infections. Iran J Pharma Res 2020;19(3):282-7.
  • 24. Al-Assil B, Mahfoud M, Hamzeh AR. First report on class 1 integrons and Trimethoprim-resistance genes from dfrA group in uropathogenic E. coli (UPEC) from the Aleppo area in Syria. Mob Gen Elements 2013;3(3):1-6. [CrossRef]
  • 25. Solberg OD, Ajiboye RM, Riley LW. Origin of class 1 and 2 integrons and gene cassettes in a population-based sample of uropathogenic Escherichia coli. J Clin Microbiol 2006;44(4):1347-51. [CrossRef]
  • 26. Zeighami H, Haghi F, Masumian N, Hemmati F, Samei A, Naderi G. Distribution of integrons and gene cassettes among uropathogenic and diarrheagenic Escherichia coli isolates in Iran. Microb Drug Resist 2015;21(4):435-40. [CrossRef]
  • 27. Halaji M, Feizi A, Mirzaei A, Sedigh Ebrahim-Saraie H, Fayyazi A, Ashraf A, et al. The Global Prevalence of Class 1 Integron and associated antibiotic resistance in Escherichia coli from patients with urinary tract infections, a systematic review and Meta-Analysis. Microb Drug Resist 2020;26(10):1208-18. [CrossRef]
  • 28. Çopur ÇA, Sandallı C, Budak EE, Yağmur G, Cizmeci Z, Ak S, et al. Characterization of class 1 and class 2 integron gene cassettes in Escherichia coli strains isolated from urine cultures: a multicenter study. Mikrobiyol Bult 2016;50(2):175- 85. [CrossRef]
  • 29. Gündoğdu A, Long YB, Vollmerhausen TL, Katouli M. Antimicrobial resistance and distribution of sul genes and integron-associated intI genes among uropathogenic Escherichia coli in Queensland, Australia. J Med Microbiol 2011;60(11):1633-42. [CrossRef]
  • 30. Düzgün AÖ, Okumuş F, Saral A, Çiçek AÇ, Cinemre S. Determination of antibiotic resistance genes and virulence factors in Escherichia coli isolated from Turkish patients with urinary tract infection. Revista da Sociedade Brasileira de Medi Tropic 2019;52:1-5. [CrossRef]
  • 31. Lee JH, Subhadra B, Son YJ, Kim DH, Park HS, Kim JM, et al. Phylogenetic group distributions, virulence factors and antimicrobial resistance properties of uropathogenic Escherichia coli strains isolated from patients with urinary tract infections in South Korea. Lett App Microbiol 2016;62(1):84-90. [CrossRef]
  • 32. Yılmaz EŞ, Aslantaş Ö. Phylogenetic group/subgroups distributions, virulence factors, and antimicrobial susceptibility of Escherichia coli strains from urinary tract infections in Hatay. Revista da Sociedade Brasileira de Medi Tropic 2020;53:1-6. [CrossRef]
Toplam 32 adet kaynakça vardır.

Ayrıntılar

Birincil Dil İngilizce
Konular Sağlık Kurumları Yönetimi
Bölüm ARAŞTIRMA
Yazarlar

Defne Gümüş 0000-0003-4070-6924

Fatma Kalaycı Yüksek 0000-0002-0028-5646

Firdevs Deniz Camadan 0000-0003-3057-6038

Merve Oral 0000-0002-7510-8441

Aslı Ceren Macunluoglu 0000-0002-6802-5998

A. Mine Küçüker 0000-0002-4809-3985

Proje Numarası 2209-a
Yayımlanma Tarihi 25 Ocak 2022
Gönderilme Tarihi 19 Ağustos 2021
Yayımlandığı Sayı Yıl 2022 Cilt: 85 Sayı: 1

Kaynak Göster

APA Gümüş, D., Kalaycı Yüksek, F., Camadan, F. D., Oral, M., vd. (2022). HIGH PREVALENCE OF CLASS I AND CLASS II INTEGRONS IN UROPATHOGENIC E. COLI STRAINS (UPECs) AND THEIR RELATIONSHIP WITH ANTIBIOTIC RESISTANCE, PHYLOGENY AND VIRULENCE. Journal of Istanbul Faculty of Medicine, 85(1), 77-85. https://doi.org/10.26650/IUITFD.984487
AMA Gümüş D, Kalaycı Yüksek F, Camadan FD, Oral M, Macunluoglu AC, Küçüker AM. HIGH PREVALENCE OF CLASS I AND CLASS II INTEGRONS IN UROPATHOGENIC E. COLI STRAINS (UPECs) AND THEIR RELATIONSHIP WITH ANTIBIOTIC RESISTANCE, PHYLOGENY AND VIRULENCE. İst Tıp Fak Derg. Ocak 2022;85(1):77-85. doi:10.26650/IUITFD.984487
Chicago Gümüş, Defne, Fatma Kalaycı Yüksek, Firdevs Deniz Camadan, Merve Oral, Aslı Ceren Macunluoglu, ve A. Mine Küçüker. “HIGH PREVALENCE OF CLASS I AND CLASS II INTEGRONS IN UROPATHOGENIC E. COLI STRAINS (UPECs) AND THEIR RELATIONSHIP WITH ANTIBIOTIC RESISTANCE, PHYLOGENY AND VIRULENCE”. Journal of Istanbul Faculty of Medicine 85, sy. 1 (Ocak 2022): 77-85. https://doi.org/10.26650/IUITFD.984487.
EndNote Gümüş D, Kalaycı Yüksek F, Camadan FD, Oral M, Macunluoglu AC, Küçüker AM (01 Ocak 2022) HIGH PREVALENCE OF CLASS I AND CLASS II INTEGRONS IN UROPATHOGENIC E. COLI STRAINS (UPECs) AND THEIR RELATIONSHIP WITH ANTIBIOTIC RESISTANCE, PHYLOGENY AND VIRULENCE. Journal of Istanbul Faculty of Medicine 85 1 77–85.
IEEE D. Gümüş, F. Kalaycı Yüksek, F. D. Camadan, M. Oral, A. C. Macunluoglu, ve A. M. Küçüker, “HIGH PREVALENCE OF CLASS I AND CLASS II INTEGRONS IN UROPATHOGENIC E. COLI STRAINS (UPECs) AND THEIR RELATIONSHIP WITH ANTIBIOTIC RESISTANCE, PHYLOGENY AND VIRULENCE”, İst Tıp Fak Derg, c. 85, sy. 1, ss. 77–85, 2022, doi: 10.26650/IUITFD.984487.
ISNAD Gümüş, Defne vd. “HIGH PREVALENCE OF CLASS I AND CLASS II INTEGRONS IN UROPATHOGENIC E. COLI STRAINS (UPECs) AND THEIR RELATIONSHIP WITH ANTIBIOTIC RESISTANCE, PHYLOGENY AND VIRULENCE”. Journal of Istanbul Faculty of Medicine 85/1 (Ocak 2022), 77-85. https://doi.org/10.26650/IUITFD.984487.
JAMA Gümüş D, Kalaycı Yüksek F, Camadan FD, Oral M, Macunluoglu AC, Küçüker AM. HIGH PREVALENCE OF CLASS I AND CLASS II INTEGRONS IN UROPATHOGENIC E. COLI STRAINS (UPECs) AND THEIR RELATIONSHIP WITH ANTIBIOTIC RESISTANCE, PHYLOGENY AND VIRULENCE. İst Tıp Fak Derg. 2022;85:77–85.
MLA Gümüş, Defne vd. “HIGH PREVALENCE OF CLASS I AND CLASS II INTEGRONS IN UROPATHOGENIC E. COLI STRAINS (UPECs) AND THEIR RELATIONSHIP WITH ANTIBIOTIC RESISTANCE, PHYLOGENY AND VIRULENCE”. Journal of Istanbul Faculty of Medicine, c. 85, sy. 1, 2022, ss. 77-85, doi:10.26650/IUITFD.984487.
Vancouver Gümüş D, Kalaycı Yüksek F, Camadan FD, Oral M, Macunluoglu AC, Küçüker AM. HIGH PREVALENCE OF CLASS I AND CLASS II INTEGRONS IN UROPATHOGENIC E. COLI STRAINS (UPECs) AND THEIR RELATIONSHIP WITH ANTIBIOTIC RESISTANCE, PHYLOGENY AND VIRULENCE. İst Tıp Fak Derg. 2022;85(1):77-85.

Contact information and address

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