HIGH PREVALENCE OF TRANSFERABLE INTEGRON-ASSOCIATED DRUG RESISTANCE IN ESCHERICHIA COLI STRAINS ISOLATED FROM BLOOD CULTURES IN A UNIVERSITY HOSPITAL IN TRABZON, TURKIYE
Year 2024,
Volume: 25 Issue: 4, 436 - 450, 22.12.2024
Ahu Reis
,
Osman Birol Özgümüş
,
Erva Rakıcı
,
İnci Durukan
,
Kurtuluş Buruk
,
Gülçin Bayramoğlu
,
Ali Osman Kılıç
Abstract
Objective: This study aimed to determine the carriage of transferable integron-associated drug resistance in
Escherichia coli (E. coli) strains isolated from blood cultures.
Materials and Methods: A total of 111 E. coli isolates were included in this study. Antimicrobial
susceptibility testing of the isolates against 17 antibiotics was performed using an automated microbiology
system. Integron-specific polymerase chain reactions (PCR) were used to detect the presence of integrons.
The antibiotic resistance gene cassettes in the variable regions of integrons were analyzed by DNA
sequencing. Plasmid transfer assays were performed using the broth mating method. The clonal
relationships among integron-carrying strains were evaluated by pulsed-field gel electrophoresis (PFGE).
Results: Resistance rates to antibiotics ranged from 0.9% to 63%. Thirty-eight strains carried gene cassettes
encoding dfrA7, dfr17-aadA5, dfrV, dfrA1-aadA1, and dfrA12-aadA2. Seven strains possessed class 2
integrons with gene arrays dfrA1-sat2-aadA1 and dfrA1-sat2-aadA30. Twenty-two integron-carrying
isolates harbored conjugative resistance plasmids, three of which were identified as belonging to the IncN
group. Two strains with class 1 integrons, isolated from different clinics, exhibited similar patterns in the
PFGE analysis.
Conclusion: Approximately 50% of E. coli isolates from blood cultures at our hospital were found to carry
integron-associated transferable drug resistance, suggesting their potential role in the horizontal
dissemination of resistance genes. Further research is needed to understand the prevalence of E. coli strains
of blood origin and the role of integrons and gene cassette arrays in the spread of resistance.
Ethical Statement
This study was approves by Karadeniz Technical University Faculty of Medicine Scientific Research Ethics Committee (Date: 12.10.2015, Decision no:3, Reference number 2015/117).
Supporting Institution
The present study was supported by the Scientific Research Project Unit of Karadeniz Technical University (Grant number: 5335/2015) as Doctoral thesis
Project Number
Grant number: 5335/2015
References
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- 2. Hastak P, Cummins ML, Gottlieb T, Cheong E, Merlino J, Myers GS, Chowdhury PR . Genomic profiling of Escherichia coli isolates from bacteraemia patients: a 3-year cohort study of isolates collected at a Sydney teaching hospital. Microbial genomics 2020; 6(5).
- 3. Lipworth S, Vihta KD, Chau K, Barker L, George S, Kavanagh J, Davies T, Vaughan A, Andersson M, Jeffery K, Oakley S, Morgan M, Hopkins S, Peto T, Crook DW, Walker AS, Stoesser N. Ten-year longitudinal molecular epidemiology study of Escherichia coli and Klebsiella species bloodstream infections in Oxfordshire, UK. Genome Medicine; 13(1): 1-13.
- 4. Aricò MO, Valletta E, Caselli D. Appropriate Use of Antibiotic and Principles of Antimicrobial Stewardship in Children. Children 2023; 10(4): 740.
- 5. Boucher Y, Labbate M, Koenig JE, Stokes HW. Integrons: mobilizable platforms that promote genetic diversity in bacteria. Trends Microbiol. 2007; 15:301–9.
- 6. Barlow RS, Gobius KS. Diverse class 2 integrons in bacteria from beef cattle sources. Journal of Antimicrobial Chemotherapy 2006; 58: 1133-1138.
- 7. Sandalli C, Buruk CK, Sancaktar M, Ozgumus OB. Prevalence of integrons and a new dfrA17 variant in Gram-negative bacilli which cause community-acquired infections. Microbiol Immunol 2010; 54: 164-169. https://doi.org/10.1111/j.1348-0421.2010.00197.x
- 8. Cicek CA, Ozgumus OB, Saral A, Sandalli C. Antimicrobial resistance patterns and integron carriage of Escherichia coli isolates causing community-acquired infections in Turkey. Annals of laboratory medicine 2014; 34(2): 139-44.
- 9. Cicek CA, Sandallı C, Budak EE, Yağmur G, Çizmeci Z, Ak S, Balcı PÖ, Şay Coşkun SU, Ay Altıntop Y, Fırat M, Sarı F, Çalışkan A, Yıldız N Sancaktar M, Özgümüş OB. İdrar Kültürlerinden İzole Edilen Escherichia coli Suşlarında Sınıf 1 ve Sınıf 2 İntegron Gen Kasetlerinin Karakterizasyonu: Çok Merkezli Bir Çalışma. Mikrobiyol Bul 2016; 50(2): 175-185.
- 10. 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 Medicina Tropical 2019; 52, e20180499.
- 11. Cicek CA, Şemen V, Ejder NA, Gündoğdu DZU, Kalcan SK, Köse FT, Özgümüş OB. Molecular epidemiological analysis of integron gene cassettes and tetA/tetB/tetD gene associations in Escherichia coli strains producing extended-spectrum β-lactamase (ESBL) in urine cultures. Advances in Clinical and Experimental Medicine 2022; 31(1): 71-79.
- 12. Wayne, PA. National Committee for Clinical Laboratory Standards. Performance standards for antimicrobial susceptibility testing. Tenth Informational supplement, M100-S10 (M2): National Committee for Clinical Laboratory Standards, 2000.
- 13. Perez-Perez FJ, Hanson ND. Detection of plasmid-mediated AmpC beta-lactamase genes in clinical isolates by using multiplex PCR. J Clin Microbiol 2002; 40(6): 2153-62.
- 14. Machado E, Canto´n R, Baquero F, Gala´n JC, Rolla´n A, Peixe L, Coque TM. Integron Content of Extended-Spectrum-Lactamase-Producing Escherichia coli Strains over 12 Years in a Single Hospital in Madrid, Spain. Antimicrobial Agents and Chemotherapy 2005; 49(5): 1823-1829.
- 15. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual (No. Ed. 2). Cold spring harbor laboratory press
- 16. Kado CI, Liu ST. Rapid procedure for detection and isolation of large and small plasmids. J Bacteriol 1981; 145(3): 1365-73.
- 17. Rohlf FJ (1993). NSYS-PC: Numerical Taxonomy and Multivariate Analysis System. New York: Exeter Software.
- 18. Mokracka J, Koczura R, Pawłowski K, Kaznowski A. Resistance patterns and integron cassette arrays of Enterobacter cloacae complex strains of human origin. Journal of Medical Microbiology 2011; 60: 737-743.
- 19. Majumdar S, Chatterjee A. Ammonium acetate induced isolation of plasmid DNA (2014) Online International Interdisciplinary Research Journal ISSN2249-9598, Volume-IV
- 20. Götz A, Pukall R, Smit E, Tietze E, Prager R, Tschäpe H, Van Elsas JD, Smalla K. Detection and characterization of broad-host-range plasmids in environmental bacteria by PCR. Applied and environmental microbiology 1996; 62(7): 2621-2628.
- 21. Durmaz R, Otlu B, Koksal F. The optimization of a rapid pulsed-field gel electrophoresis protocol for the typing of Acinetobacter baumannii, Escherichia coli and Klebsiella spp. Jpn J Infect Dis 2009; 62: 372–377.
- 22. Ibrahim DR, Dodd CE, Stekel DJ, Meshioye RT, Diggle M, Lister M, Hobman JL. Multidrug-Resistant ESBL-Producing E. coli in Clinical Samples from the UK. Antibiotics 2023; 12(1): 169.
- 23. Birru M, Woldemariam M, Manilal A, Aklilu A, Tsalla T, Mitiku A, Gezmu T. Bacterial profile, antimicrobial susceptibility patterns, and associated factors among bloodstream infection suspected patients attending Arba Minch General Hospital, Ethiopia. Scientific reports 2021; 11(1): 1-13.
- 24. Duran H, Çeken N, Atik B. Escherichia coli ve Klebsiella pneumoniae Türlerinde Antibiyotik Direnci ne Durumda? Yoğun Bakım Ünitesinden Beş Yıllık Analiz. Fırat Tıp Dergisi/Firat Med J 2022; 27(2): 116-120
- 25. Son T, Manh ND, Trung NT, Quyen DT, Meyer CG, Phuong NTK, Hoan PQ, Sang VV, Nurjadi D, Velavan T, Bang MH, Song LH. Molecular detection of blaCTX-M gene to predict phenotypic cephalosporin resistance and clinical outcome of Escherichia coli bloodstream infections in Vietnam. Annals of clinical microbiology and antimicrobials 2021; 20(1): 1-9.
- 26. Kreidl P, Kirchner T, Fille M, Heller I, Lass-Flörl C, Orth-Höller D. Antibiotic resistance of blood cultures in regional and tertiary hospital settings of Tyrol, Austria (2006-2015): Impacts & trends. PloS one 2019; 14(10): e0223467.
- 27. Anvarinejad M, Khalifeh M, Mardaneh J, Pouladfar G, Dehyadegari MA. Bloodstream infections in the south of Iran: microbiological profile and antibiotic-resistance patterns of isolated bacteria. Crescent J Med Biol Sci 2021; 8(4): 312-318.
- 28. Hu LF, Chang X, Ye Y, Wang ZX, Shao YB, Shi W, Li X, Li JB. Stenotrophomonas maltophilia resistance to trimethoprim/sulfamethoxazole mediated by acquisition of sul and dfrA genes in a plasmid-mediated class 1 integron. Int J Antimicrob Agents 2011; 37(3): 230-4.
- 29. Sacristán C, Esperón F, Herrera-León S, Iglesias I, Neves E, Nogal V, Muñoz MJ, de la Torre A. Virulence genes, antibiotic resistance and integrons in Escherichia coli strains isolated from synanthropic birds from Spain. Avian Pathol 2014; 43(2): 172-5.
- 30. Zhu W, Wang T, Zhu Y, Xiao L, Liu W, Wei Q. Two-dimensional PCR for detecting class 1, 2 and 3 integrons. Heliyon 2022; 8(11): e11844.
- 31. Başkan C, Sırıken B, Tüfekci EF, Kılınç Ç, Ertürk Ö, Erol İ (2022) Presence of quorum sensing system, virulence genes, biofilm formation and relationship among them and class 1 integron in carbapenem-resistant clinical Pseudomonas aeruginosa isolates. Archives of Microbiology 2022; 204(8): 464.
- 32. Rakici E, Altunisik A, Sahin K, Ozgumus OB. Determination and molecular analysis of antibiotic resistance in Gram-negative enteric bacteria isolated from Pelophylax sp. in the Eastern Black Sea Region. Acta Veterinaria Hungarica 2021; 69(3): 223-233.
- 33. Sivri N, Sandalli C, Ozgumus OB, Colakoglu F, Dogan D. Antibiotic resistance profiles of enteric bacteria isolated from Kucukcekmece Lagoon (Istanbul-Turkey). Turkish Journal of Fisheries and Aquatic Sciences 2012; 12(3).
- 34. Liu W, Zhao F, Chen J. Analysis of drug resistance genes of integrons in clinical isolates of Escherichia coli from elderly bloodstream infections. Cellular and Molecular Biology 2022; 68(6): 67-72.
- 35. Abdel-Rhman SH, Elbargisy RM, Rizk DE. Characterization of integrons and quinolone resistance in clinical Escherichia coli isolates in Mansoura City, Egypt. International Journal of Microbiology 2021.
- 36. Dehkordi MK, Halaji M, Nouri S. Prevalence of class 1 integron in Escherichia coli isolated from animal sources in Iran: a systematic review and meta-analysis. Tropical Medicine and Health 2020; 48:16.
- 37. Ahumada-Santos YP, Báez-Flores ME, Díaz-Camacho SP, de Jesús Uribe-Beltrán M, Eslava-Campos CA, Parra-Unda JR, Delgado-Vargas F. Association of phylogenetic distribution and presence of integrons with multidrug resistance in Escherichia coli clinical isolates from children with diarrhoea. Journal of Infection and Public Health 2020; 13(5): 767-772.
- 38. Partridge SR, Tsafnat G, Coiera E, Iredell JR. Gene cassettes and cassette arrays inmobile resistance integrons. FEMS Microbiol Rev 2009; 33(4): 757-784.
- 39. Ndi OL, Barton MD. Incidence of class 1 integron and other antibiotic resistance determinants in Aeromonas spp. from rainbow trout farms in Australia. J Fish Dis 2011; 34(8): 589-99.
- 40. Szmolka A, Nagy B. Multi drug resistant commensal Escherichia coli in animals and its impact for public health. Frontier in microbiology 2013; 4: 258. https://doi.org/10.3389/fmicb.2013.00258
- 41. Düzgün AÖ, Saral A (2018) Investigation of Antibiotic Resistance Genes and Class 1 Integron in Multi-Drug Resistant P. aeruginosa and E. coli Strains. Cumhuriyet Sci. J. 2018; Vol. 39-4: 1063-1068.
- 42. Chen J, Su Z, Liu Y, Wang S, Dai X, Li Y, Peng S, Shao Q, Zhang H, Wen P, Yu J, Huang X, Xu H. Identification and characterization of class 1 integrons among Pseudomonas aeruginosa isolates from patients in Zhenjiang, China. International Journal of Infectious Diseases 2009; 13(6): 717-721.
- 43. Schlüter A, Szczepanowski R, Pühler A, Top EM. Genomics of IncP-1antibiotic resistance plasmids isolated from wastewater treatment plants provides evidence forawidely accessible drug resistance gene pool. FEMS Microbiol Rev 2007; 31: 449-477.
Trabzon, Türkiyedeki Bir Üniversite Hastanesinde Kan Kültürlerinden İzole Edilen Escherichia coli Suşlarında Transfer Edilebilir İntegronla İlişkili İlaç Direncinin Yüksek Prevalansı
Year 2024,
Volume: 25 Issue: 4, 436 - 450, 22.12.2024
Ahu Reis
,
Osman Birol Özgümüş
,
Erva Rakıcı
,
İnci Durukan
,
Kurtuluş Buruk
,
Gülçin Bayramoğlu
,
Ali Osman Kılıç
Abstract
Giriş: Bu çalışmada, Karadeniz Teknik Üniversitesi Hastanesi Araştırma ve Uygulama Merkezi'nde kan kültürlerinden izole edilen Escherichia coli (E. coli) suşlarının transfer edilebilir integron ilişkili ilaç direncine sahip olup olmadığının belirlenmesi amaçlanmıştır.
Materyal ve Metod: İntegronların varlığı, integrona özgü polimeraz zincir reaksiyonları ile belirlendi ve amplikonlar, DNA dizilimi ile analiz edildi. Plazmid transfer deneyleri, sıvıda çiftleşme yöntemiyle gerçekleştirildi. İntegron içeren suşların klonal ilişkisi pulsed field jel elektroforezi (PFGE) ile değerlendirildi.
Bulgular: Kullanılan antibiyotik gruplarına direnç oranları %0,9 ile %63 arasındaydı. Otuz sekiz (%34,2) suş, dfrA7, dfr17-aadA5, dfrV, dfrA1-aadA1 ve dfrA12-aadA2 gen kaset dizilerini taşıyan sınıf 1 integronları içeriyordu. Yedi (%6,3) suş, dfrA1-sat2-aadA1 ve dfrA1-sat2-aadA30 gen kaset dizilerine sahip sınıf 2 integronları içeriyordu. İntegron taşıyan izolatlarda 22 konjugatif direnç plazmidi barındırıldı ve bunlardan üçünün IncN grubunda olduğu belirlendi. Farklı kliniklerden izole edilen sınıf 1 integronları taşıyan dört suş, PFGE analizinde klonal olarak benzer modeller gösterdi.
Sonuç: Hastanemizdeki E. coli izolatlarının yaklaşık %50'sinin integronla ilişkili aktarılabilir ilaç direnci taşıdığı ve yatay yayılımda önemli bir rol oynayabileceği sonucuna vardık. Bu hastanede ve ülke genelinde kan kökenli E. coli suşlarında integronların taşınması arasındaki ilişkinin açıklanabilmesi için daha ileri moleküler epidemiyolojik araştırmalara ihtiyaç vardır.
Project Number
Grant number: 5335/2015
References
- 1. Delle RD, Pezzotti P, Fontana C, Altieri A, Minelli S, Mariotti B, Cerretti R, Leoni D, Andreoni M, Sarmati L. An in-depth analysis of nosocomial bloodstream infections due to Gram-negative bacilli: clinical features, microbiological characteristics and predictors of mortality in a 1 year, prospective study in a large tertiary care Italian hospital. Infectious Diseases 2019; 51(1): 12-22.
- 2. Hastak P, Cummins ML, Gottlieb T, Cheong E, Merlino J, Myers GS, Chowdhury PR . Genomic profiling of Escherichia coli isolates from bacteraemia patients: a 3-year cohort study of isolates collected at a Sydney teaching hospital. Microbial genomics 2020; 6(5).
- 3. Lipworth S, Vihta KD, Chau K, Barker L, George S, Kavanagh J, Davies T, Vaughan A, Andersson M, Jeffery K, Oakley S, Morgan M, Hopkins S, Peto T, Crook DW, Walker AS, Stoesser N. Ten-year longitudinal molecular epidemiology study of Escherichia coli and Klebsiella species bloodstream infections in Oxfordshire, UK. Genome Medicine; 13(1): 1-13.
- 4. Aricò MO, Valletta E, Caselli D. Appropriate Use of Antibiotic and Principles of Antimicrobial Stewardship in Children. Children 2023; 10(4): 740.
- 5. Boucher Y, Labbate M, Koenig JE, Stokes HW. Integrons: mobilizable platforms that promote genetic diversity in bacteria. Trends Microbiol. 2007; 15:301–9.
- 6. Barlow RS, Gobius KS. Diverse class 2 integrons in bacteria from beef cattle sources. Journal of Antimicrobial Chemotherapy 2006; 58: 1133-1138.
- 7. Sandalli C, Buruk CK, Sancaktar M, Ozgumus OB. Prevalence of integrons and a new dfrA17 variant in Gram-negative bacilli which cause community-acquired infections. Microbiol Immunol 2010; 54: 164-169. https://doi.org/10.1111/j.1348-0421.2010.00197.x
- 8. Cicek CA, Ozgumus OB, Saral A, Sandalli C. Antimicrobial resistance patterns and integron carriage of Escherichia coli isolates causing community-acquired infections in Turkey. Annals of laboratory medicine 2014; 34(2): 139-44.
- 9. Cicek CA, Sandallı C, Budak EE, Yağmur G, Çizmeci Z, Ak S, Balcı PÖ, Şay Coşkun SU, Ay Altıntop Y, Fırat M, Sarı F, Çalışkan A, Yıldız N Sancaktar M, Özgümüş OB. İdrar Kültürlerinden İzole Edilen Escherichia coli Suşlarında Sınıf 1 ve Sınıf 2 İntegron Gen Kasetlerinin Karakterizasyonu: Çok Merkezli Bir Çalışma. Mikrobiyol Bul 2016; 50(2): 175-185.
- 10. 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 Medicina Tropical 2019; 52, e20180499.
- 11. Cicek CA, Şemen V, Ejder NA, Gündoğdu DZU, Kalcan SK, Köse FT, Özgümüş OB. Molecular epidemiological analysis of integron gene cassettes and tetA/tetB/tetD gene associations in Escherichia coli strains producing extended-spectrum β-lactamase (ESBL) in urine cultures. Advances in Clinical and Experimental Medicine 2022; 31(1): 71-79.
- 12. Wayne, PA. National Committee for Clinical Laboratory Standards. Performance standards for antimicrobial susceptibility testing. Tenth Informational supplement, M100-S10 (M2): National Committee for Clinical Laboratory Standards, 2000.
- 13. Perez-Perez FJ, Hanson ND. Detection of plasmid-mediated AmpC beta-lactamase genes in clinical isolates by using multiplex PCR. J Clin Microbiol 2002; 40(6): 2153-62.
- 14. Machado E, Canto´n R, Baquero F, Gala´n JC, Rolla´n A, Peixe L, Coque TM. Integron Content of Extended-Spectrum-Lactamase-Producing Escherichia coli Strains over 12 Years in a Single Hospital in Madrid, Spain. Antimicrobial Agents and Chemotherapy 2005; 49(5): 1823-1829.
- 15. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual (No. Ed. 2). Cold spring harbor laboratory press
- 16. Kado CI, Liu ST. Rapid procedure for detection and isolation of large and small plasmids. J Bacteriol 1981; 145(3): 1365-73.
- 17. Rohlf FJ (1993). NSYS-PC: Numerical Taxonomy and Multivariate Analysis System. New York: Exeter Software.
- 18. Mokracka J, Koczura R, Pawłowski K, Kaznowski A. Resistance patterns and integron cassette arrays of Enterobacter cloacae complex strains of human origin. Journal of Medical Microbiology 2011; 60: 737-743.
- 19. Majumdar S, Chatterjee A. Ammonium acetate induced isolation of plasmid DNA (2014) Online International Interdisciplinary Research Journal ISSN2249-9598, Volume-IV
- 20. Götz A, Pukall R, Smit E, Tietze E, Prager R, Tschäpe H, Van Elsas JD, Smalla K. Detection and characterization of broad-host-range plasmids in environmental bacteria by PCR. Applied and environmental microbiology 1996; 62(7): 2621-2628.
- 21. Durmaz R, Otlu B, Koksal F. The optimization of a rapid pulsed-field gel electrophoresis protocol for the typing of Acinetobacter baumannii, Escherichia coli and Klebsiella spp. Jpn J Infect Dis 2009; 62: 372–377.
- 22. Ibrahim DR, Dodd CE, Stekel DJ, Meshioye RT, Diggle M, Lister M, Hobman JL. Multidrug-Resistant ESBL-Producing E. coli in Clinical Samples from the UK. Antibiotics 2023; 12(1): 169.
- 23. Birru M, Woldemariam M, Manilal A, Aklilu A, Tsalla T, Mitiku A, Gezmu T. Bacterial profile, antimicrobial susceptibility patterns, and associated factors among bloodstream infection suspected patients attending Arba Minch General Hospital, Ethiopia. Scientific reports 2021; 11(1): 1-13.
- 24. Duran H, Çeken N, Atik B. Escherichia coli ve Klebsiella pneumoniae Türlerinde Antibiyotik Direnci ne Durumda? Yoğun Bakım Ünitesinden Beş Yıllık Analiz. Fırat Tıp Dergisi/Firat Med J 2022; 27(2): 116-120
- 25. Son T, Manh ND, Trung NT, Quyen DT, Meyer CG, Phuong NTK, Hoan PQ, Sang VV, Nurjadi D, Velavan T, Bang MH, Song LH. Molecular detection of blaCTX-M gene to predict phenotypic cephalosporin resistance and clinical outcome of Escherichia coli bloodstream infections in Vietnam. Annals of clinical microbiology and antimicrobials 2021; 20(1): 1-9.
- 26. Kreidl P, Kirchner T, Fille M, Heller I, Lass-Flörl C, Orth-Höller D. Antibiotic resistance of blood cultures in regional and tertiary hospital settings of Tyrol, Austria (2006-2015): Impacts & trends. PloS one 2019; 14(10): e0223467.
- 27. Anvarinejad M, Khalifeh M, Mardaneh J, Pouladfar G, Dehyadegari MA. Bloodstream infections in the south of Iran: microbiological profile and antibiotic-resistance patterns of isolated bacteria. Crescent J Med Biol Sci 2021; 8(4): 312-318.
- 28. Hu LF, Chang X, Ye Y, Wang ZX, Shao YB, Shi W, Li X, Li JB. Stenotrophomonas maltophilia resistance to trimethoprim/sulfamethoxazole mediated by acquisition of sul and dfrA genes in a plasmid-mediated class 1 integron. Int J Antimicrob Agents 2011; 37(3): 230-4.
- 29. Sacristán C, Esperón F, Herrera-León S, Iglesias I, Neves E, Nogal V, Muñoz MJ, de la Torre A. Virulence genes, antibiotic resistance and integrons in Escherichia coli strains isolated from synanthropic birds from Spain. Avian Pathol 2014; 43(2): 172-5.
- 30. Zhu W, Wang T, Zhu Y, Xiao L, Liu W, Wei Q. Two-dimensional PCR for detecting class 1, 2 and 3 integrons. Heliyon 2022; 8(11): e11844.
- 31. Başkan C, Sırıken B, Tüfekci EF, Kılınç Ç, Ertürk Ö, Erol İ (2022) Presence of quorum sensing system, virulence genes, biofilm formation and relationship among them and class 1 integron in carbapenem-resistant clinical Pseudomonas aeruginosa isolates. Archives of Microbiology 2022; 204(8): 464.
- 32. Rakici E, Altunisik A, Sahin K, Ozgumus OB. Determination and molecular analysis of antibiotic resistance in Gram-negative enteric bacteria isolated from Pelophylax sp. in the Eastern Black Sea Region. Acta Veterinaria Hungarica 2021; 69(3): 223-233.
- 33. Sivri N, Sandalli C, Ozgumus OB, Colakoglu F, Dogan D. Antibiotic resistance profiles of enteric bacteria isolated from Kucukcekmece Lagoon (Istanbul-Turkey). Turkish Journal of Fisheries and Aquatic Sciences 2012; 12(3).
- 34. Liu W, Zhao F, Chen J. Analysis of drug resistance genes of integrons in clinical isolates of Escherichia coli from elderly bloodstream infections. Cellular and Molecular Biology 2022; 68(6): 67-72.
- 35. Abdel-Rhman SH, Elbargisy RM, Rizk DE. Characterization of integrons and quinolone resistance in clinical Escherichia coli isolates in Mansoura City, Egypt. International Journal of Microbiology 2021.
- 36. Dehkordi MK, Halaji M, Nouri S. Prevalence of class 1 integron in Escherichia coli isolated from animal sources in Iran: a systematic review and meta-analysis. Tropical Medicine and Health 2020; 48:16.
- 37. Ahumada-Santos YP, Báez-Flores ME, Díaz-Camacho SP, de Jesús Uribe-Beltrán M, Eslava-Campos CA, Parra-Unda JR, Delgado-Vargas F. Association of phylogenetic distribution and presence of integrons with multidrug resistance in Escherichia coli clinical isolates from children with diarrhoea. Journal of Infection and Public Health 2020; 13(5): 767-772.
- 38. Partridge SR, Tsafnat G, Coiera E, Iredell JR. Gene cassettes and cassette arrays inmobile resistance integrons. FEMS Microbiol Rev 2009; 33(4): 757-784.
- 39. Ndi OL, Barton MD. Incidence of class 1 integron and other antibiotic resistance determinants in Aeromonas spp. from rainbow trout farms in Australia. J Fish Dis 2011; 34(8): 589-99.
- 40. Szmolka A, Nagy B. Multi drug resistant commensal Escherichia coli in animals and its impact for public health. Frontier in microbiology 2013; 4: 258. https://doi.org/10.3389/fmicb.2013.00258
- 41. Düzgün AÖ, Saral A (2018) Investigation of Antibiotic Resistance Genes and Class 1 Integron in Multi-Drug Resistant P. aeruginosa and E. coli Strains. Cumhuriyet Sci. J. 2018; Vol. 39-4: 1063-1068.
- 42. Chen J, Su Z, Liu Y, Wang S, Dai X, Li Y, Peng S, Shao Q, Zhang H, Wen P, Yu J, Huang X, Xu H. Identification and characterization of class 1 integrons among Pseudomonas aeruginosa isolates from patients in Zhenjiang, China. International Journal of Infectious Diseases 2009; 13(6): 717-721.
- 43. Schlüter A, Szczepanowski R, Pühler A, Top EM. Genomics of IncP-1antibiotic resistance plasmids isolated from wastewater treatment plants provides evidence forawidely accessible drug resistance gene pool. FEMS Microbiol Rev 2007; 31: 449-477.