Phylogenetic groups, serogroups and virulence factors of uropathogenic Escherichia coli isolated from patients with urinary tract infection in Baghdad, Iraq
Abstract
Background and Objectives: Uropathogenic Escherichia coli (UPEC) is divided into different phylogenetic groups that differ in their antibiotic resistance patterns, serogroups and pathogenicity. This study aimed to investigate the prevalence of phylogenetic groups of UPEC isolates and their relationship with serogroups and virulence factors in patients with UTIs.
Materials and Methods: Of the 412 urine samples tested a total of 150 UPEC were isolated and confirmed with PCR using 16S rRNA gene. Antibiotic resistance of the isolates was tested using disk diffusion method and the isolates were divided into phylogenetic groups by the quadruplex PCR method. The prevalence of serogroups and virulence genes were investigated using multiplex PCR.
Results: 87 (58%) of the isolates belonged to phylogroup B2. Virulence genes fimH (95.3%), aer (49.3%) and serogroups O8 (22.3%), O25 (21.5%) showed the highest prevalence. The lowest drug resistance was observed against imipenem (4.6%) and meropenem (3.3%). The prevalence of multidrug-resistant and extended-spectrum beta-lactamases isolates were 60% and 61.3%, respectively. We also found a significant relationship between phylogenetic groups, serogroups and virulence factors among our isolates.
Conclusion: The high abundance of phylogenetic group B2, serogroups O8 and O25, and virulence genes fimH and aer indicate their importance in the pathogenesis of UPEC in this country.
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2. Shah C, Baral R, Bartaula B, Shrestha LB. Virulence factors of uropathogenic Escherichia coli (UPEC) and correlation with antimicrobial resistance. BMC Microbiol 2019; 19: 204.
3. Ambite I, Butler D, Wan MLY, Rosenblad T, Tran TH, Chao SM, et al. Molecular determinants of disease severity in urinary tract infection. Nat Rev Urol 2021; 18: 468-486.
4. Cristea VC, Gheorghe I, Czobor Barbu I, Popa LI, Ispas B, Grigore G A, et al. Snapshot of phylogenetic groups, virulence, and resistance markers in Escherichia coli uropathogenic strains isolated from outpatients with urinary tract infections in Bucharest, Romania. Biomed Res Int 2019; 2019: 5712371.
5. Serretiello E, Folliero V, Santella B, Giordano G, Santoro E, De Caro F, et al. Trend of bacterial uropathogens and their susceptibility pattern: study of single academic high-volume center in Italy (2015–2019). Int J Microbiol 2021; 2021: 5541706.
6. Clermont O, Bonacorsi S, Bingen E. Rapid and simple determination of the Escherichia coli phylogenetic group. Appl Environ Microbiol 2000; 66: 4555-4558.
7. Clermont O, Christenson J K, Denamur E, Gordon DM. The Clermont Escherichia coli phylo-typing method revisited: improvement of specificity and detection of new phylo-groups. Environ Microbiol Rep 2013; 5: 58-65.
8. Noie Oskouie A, Hasani A, Ahangarzadeh Rezaee M, Soroush Bar Haghi MH, Hasani A, Soltani E. A relationship between O-serotype, antibiotic susceptibility and biofilm formation in Uropathogenic Escherichia coli. Microb Drug Resist 2019; 25: 951-958.
9. Rezatofighi SE, Mirzarazi M, Salehi M. Virulence genes and phylogenetic groups of uropathogenic Escherichia coli isolates from patients with urinary tract infection and uninfected control subjects: a case-control study. BMC Infect Dis 2021; 21: 361.
10. Abe CM, Salvador FA, Falsetti IN, Vieira MAM, Blanco J, Blanco JE, et al. Uropathogenic Escherichia coli (UPEC) strains may carry virulence properties of diarrhoeagenic E. coli. FEMS Immunol Med Microbiol 2008; 52: 397-406.
11. Yamamoto S. Molecular epidemiology of uropathogenic Escherichia coli. J Infect Chemother 2007; 13: 68-73.
12. Yılmaz EŞ, Aslantaş Ö. Phylogenetic group/subgroups distributions, virulence factors, and antimicrobial susceptibility of Escherichia coli strains from urinary tract infections in hatay. Rev Soc Bras Med Trop 2020; 53:e20190429.
13. Liu B, Furevi A, Perepelov AV, Guo X, Cao H, Wang Q, et al. Structure and genetics of Escherichia coli O antigens. FEMS Microbiol Rev 2020; 44: 655-683.
14. Dadi BR, Abebe T, Zhang L, Mihret A, Abebe W, Amogne W. Distribution of virulence genes and phylogenetics of uropathogenic Escherichia coli among urinary tract infection patients in Addis Ababa, Ethiopia. BMC Infect Dis 2020; 20: 108.
15. Allami M, Bahreini M, Sharifmoghadam MR. Antibiotic resistance, phylogenetic typing, and virulence genes profile analysis of uropathogenic Escherichia coli isolated from patients in southern Iraq. J Appl Genet 2022; 63: 401-412.
16. Mohammed EJ, Allami M, Sharifmoghadam MR, Bahreini M. Relationship between antibiotic resistance patterns and O-serogroups in uropathogenic Escherichia coli strains isolated from Iraqi patients. Jundishapur J Microbiol 2021; 14(8):e118833.
17. Momtaz H, Karimian A, Madani M, Dehkordi FS, Ranjbar R, Sarshar M, et al. Uropathogenic Escherichia coli in Iran: serogroup distributions, virulence factors and antimicrobial resistance properties. Ann Clin Microbiol Antimicrob 2013; 12: 8.
18. Düzgün AÖ, Okumuş F, Saral A, Çiçek A Ç, Cinemre S. Determination of antibiotic resistance genes and virulence factors in Escherichia coli isolated from Turkish patients with urinary tract infection. Rev Soc Bras Med Trop 2019; 52:e20180499.
19. Al-Naqshbandi AA, Chawsheen MA, Abdulqader HH. Prevalence and antimicrobial susceptibility of bacterial pathogens isolated from urine specimens received in rizgary hospital-Erbil. J Infect Public Health 2019; 12: 330-336.
20. Tewawong N, Kowaboot S, Pimainog Y, Watanagul N, Thongmee T, Poovorawan Y. Distribution of phylogenetic groups, adhesin genes, biofilm formation, and antimicrobial resistance of uropathogenic Escherichia coli isolated from hospitalized patients in Thailand. PeerJ 2020; 8: e10453.
21. Sharma S, Kaur N, Malhotra S, Madan P, Ahmad W, Hans C. Serotyping and antimicrobial susceptibility pattern of Escherichia coli isolates from urinary tract infections in pediatric population in a tertiary care hospital. J Pathog 2016; 2016: 2548517.
22. Shrestha R, Khanal S, Poudel P, Khadayat K, Ghaju S, Bhandari A, et al. Extended spectrum β-lactamase producing uropathogenic Escherichia coli and the correlation of biofilm with antibiotics resistance in Nepal. Ann Clin Microbiol Antimicrob 2019; 18: 42.
23. Halabi MK, Lahlou FA, Diawara I, El Adouzi Y, Marnaoui R, Benmessaoud R, et al. Antibiotic resistance pattern of extended spectrum Beta Lactamase producing Escherichia coli isolated from patients with urinary tract infection in Morocco. Front Cell Infect Microbiol 2021; 11: 720701.
24. Singh N, Pattnaik D, Neogi DK, Jena J, Mallick B. Prevalence of ESBL in Escherichia coli isolates among ICU patients in a tertiary care hospital. J Clin Diagn Res 2016; 10: DC19-DC22.
25. Ballesteros-Monrreal MG, Arenas-Hernández MM, Enciso-Martínez Y, Martínez-de la Peña C F, Del C Rocha-Gracia R, Lozano-Zarain P, et al. Virulence and resistance determinants of uropathogenic Escherichia coli strains isolated from pregnant and non-pregnant women from two states in Mexico. Infect Drug Resist 2020; 13: 295-310.
26. Wang Y, Zhao S, Han L, Guo X, Chen M, Ni Y, et al. Drug resistance and virulence of uropathogenic Escherichia coli from Shanghai, China. J Antibiot (Tokyo) 2014; 67: 799-805.
27. Lee DS, Lee SJ, Choe HS. Community-acquired urinary tract infection by Escherichia coli in the era of antibiotic resistance. Biomed Res Int 2018; 2018: 7656752.
28. Ndzime YM, Onanga R, Kassa RFK, Bignoumba M, Nguema PPM, Gafou A, et al. Epidemiology of community origin Escherichia coli and uropathogenic strains resistant to antibiotics in Franceville, Gabon. Infect Drug Resist 2021; 14: 585-594.
29. Ventola CL. The antibiotic resistance crisis: part 1: causes and threats. P T 2015; 40: 277-283.
30. Petca RC, Negoiță S, Mareș C, Petca A, Popescu RI, Chibelean CB. Heterogeneity of antibiotics multidrug-resistance profile of uropathogens in Romanian population. Antibiotics (Basel) 2021; 10: 523.
31. Tenney J, Hudson N, Alnifaidy H, Li JTC, Fung KH. Risk factors for aquiring multidrug-resistant organisms in urinary tract infections: a systematic literature review. Saudi Pharm J 2018; 26: 678-684.
32. Boroumand M, Naghmachi M, Ghatee MA. Detection of phylogenetic groups and drug resistance genes of Escherichia coli causing urinary tract infection in southwest Iran. Jundishapur J Microbiol 2021; 14(2):e112547.
33. Sokurenko EV, Chesnokova V, Dykhuizen DE, Ofek I, Wu XR, Krogfelt KA, et al. Pathogenic adaptation of Escherichia coli by natural variation of the FimH adhesin. Proc Natl Acad Sci U S A 1998; 95: 8922-8926.
34. Sabaté M, Moreno E, Pérez T, Andreu A, Prats G. Pathogenicity island markers in commensal and uropathogenic Escherichia coli isolates. Clin Microbiol Infect 2006; 12: 880-886.
35. Chakraborty A, Saralaya V, Adhikari P, Shenoy S, Baliga S, Hegde A. Characterization of Escherichia coli phylogenetic groups associated with extraintestinal infections in South Indian population. Ann Med Health Sci Res 2015; 5: 241-246.
36. Hernández-Chiñas U, Pérez-Ramos A, Belmont-Monroy L, Chávez-Berrocal ME, González-Villalobos E, Navarro-Ocaña A, et al. Characterization of auto-agglutinating and non-typeable uropathogenic Escherichia coli strains. J Infect Dev Ctries 2019; 13: 465-472.
37. Dadi BR, Abebe T, Zhang L, Mihret A, Abebe W, Amogne W. Drug resistance and plasmid profile of uropathogenic Escherichia coli among urinary tract infection patients in Addis Abeba. J Infect Dev Ctries 2018; 12: 608-615.
38. Terlizzi ME, Gribaudo G, Maffei ME. UroPathogenic Escherichia coli (UPEC) infections: virulence factors, bladder responses, antibiotic, and non-antibiotic antimicrobial strategies. Front Microbiol 2017; 8: 1566.
39. Tabasi M, Karam M R A, Habibi M, Mostafavi E, Bouzari S. Genotypic characterization of virulence factors in Escherichia coli isolated from patients with acute cystitis, pyelonephritis and asymptomatic bacteriuria. J Clin Diagn Res 2016; 10: DC01-DC07.
40. Ghavidel M, Gholamhosseini-Moghadam T, Nourian K, Ghazvini K. Virulence factors analysis and antibiotic resistance of uropathogenic Escherichia coli isolated from patients in northeast of Iran. Iran J Microbiol 2020; 12: 223-230.
2. Shah C, Baral R, Bartaula B, Shrestha LB. Virulence factors of uropathogenic Escherichia coli (UPEC) and correlation with antimicrobial resistance. BMC Microbiol 2019; 19: 204.
3. Ambite I, Butler D, Wan MLY, Rosenblad T, Tran TH, Chao SM, et al. Molecular determinants of disease severity in urinary tract infection. Nat Rev Urol 2021; 18: 468-486.
4. Cristea VC, Gheorghe I, Czobor Barbu I, Popa LI, Ispas B, Grigore G A, et al. Snapshot of phylogenetic groups, virulence, and resistance markers in Escherichia coli uropathogenic strains isolated from outpatients with urinary tract infections in Bucharest, Romania. Biomed Res Int 2019; 2019: 5712371.
5. Serretiello E, Folliero V, Santella B, Giordano G, Santoro E, De Caro F, et al. Trend of bacterial uropathogens and their susceptibility pattern: study of single academic high-volume center in Italy (2015–2019). Int J Microbiol 2021; 2021: 5541706.
6. Clermont O, Bonacorsi S, Bingen E. Rapid and simple determination of the Escherichia coli phylogenetic group. Appl Environ Microbiol 2000; 66: 4555-4558.
7. Clermont O, Christenson J K, Denamur E, Gordon DM. The Clermont Escherichia coli phylo-typing method revisited: improvement of specificity and detection of new phylo-groups. Environ Microbiol Rep 2013; 5: 58-65.
8. Noie Oskouie A, Hasani A, Ahangarzadeh Rezaee M, Soroush Bar Haghi MH, Hasani A, Soltani E. A relationship between O-serotype, antibiotic susceptibility and biofilm formation in Uropathogenic Escherichia coli. Microb Drug Resist 2019; 25: 951-958.
9. Rezatofighi SE, Mirzarazi M, Salehi M. Virulence genes and phylogenetic groups of uropathogenic Escherichia coli isolates from patients with urinary tract infection and uninfected control subjects: a case-control study. BMC Infect Dis 2021; 21: 361.
10. Abe CM, Salvador FA, Falsetti IN, Vieira MAM, Blanco J, Blanco JE, et al. Uropathogenic Escherichia coli (UPEC) strains may carry virulence properties of diarrhoeagenic E. coli. FEMS Immunol Med Microbiol 2008; 52: 397-406.
11. Yamamoto S. Molecular epidemiology of uropathogenic Escherichia coli. J Infect Chemother 2007; 13: 68-73.
12. Yılmaz EŞ, Aslantaş Ö. Phylogenetic group/subgroups distributions, virulence factors, and antimicrobial susceptibility of Escherichia coli strains from urinary tract infections in hatay. Rev Soc Bras Med Trop 2020; 53:e20190429.
13. Liu B, Furevi A, Perepelov AV, Guo X, Cao H, Wang Q, et al. Structure and genetics of Escherichia coli O antigens. FEMS Microbiol Rev 2020; 44: 655-683.
14. Dadi BR, Abebe T, Zhang L, Mihret A, Abebe W, Amogne W. Distribution of virulence genes and phylogenetics of uropathogenic Escherichia coli among urinary tract infection patients in Addis Ababa, Ethiopia. BMC Infect Dis 2020; 20: 108.
15. Allami M, Bahreini M, Sharifmoghadam MR. Antibiotic resistance, phylogenetic typing, and virulence genes profile analysis of uropathogenic Escherichia coli isolated from patients in southern Iraq. J Appl Genet 2022; 63: 401-412.
16. Mohammed EJ, Allami M, Sharifmoghadam MR, Bahreini M. Relationship between antibiotic resistance patterns and O-serogroups in uropathogenic Escherichia coli strains isolated from Iraqi patients. Jundishapur J Microbiol 2021; 14(8):e118833.
17. Momtaz H, Karimian A, Madani M, Dehkordi FS, Ranjbar R, Sarshar M, et al. Uropathogenic Escherichia coli in Iran: serogroup distributions, virulence factors and antimicrobial resistance properties. Ann Clin Microbiol Antimicrob 2013; 12: 8.
18. Düzgün AÖ, Okumuş F, Saral A, Çiçek A Ç, Cinemre S. Determination of antibiotic resistance genes and virulence factors in Escherichia coli isolated from Turkish patients with urinary tract infection. Rev Soc Bras Med Trop 2019; 52:e20180499.
19. Al-Naqshbandi AA, Chawsheen MA, Abdulqader HH. Prevalence and antimicrobial susceptibility of bacterial pathogens isolated from urine specimens received in rizgary hospital-Erbil. J Infect Public Health 2019; 12: 330-336.
20. Tewawong N, Kowaboot S, Pimainog Y, Watanagul N, Thongmee T, Poovorawan Y. Distribution of phylogenetic groups, adhesin genes, biofilm formation, and antimicrobial resistance of uropathogenic Escherichia coli isolated from hospitalized patients in Thailand. PeerJ 2020; 8: e10453.
21. Sharma S, Kaur N, Malhotra S, Madan P, Ahmad W, Hans C. Serotyping and antimicrobial susceptibility pattern of Escherichia coli isolates from urinary tract infections in pediatric population in a tertiary care hospital. J Pathog 2016; 2016: 2548517.
22. Shrestha R, Khanal S, Poudel P, Khadayat K, Ghaju S, Bhandari A, et al. Extended spectrum β-lactamase producing uropathogenic Escherichia coli and the correlation of biofilm with antibiotics resistance in Nepal. Ann Clin Microbiol Antimicrob 2019; 18: 42.
23. Halabi MK, Lahlou FA, Diawara I, El Adouzi Y, Marnaoui R, Benmessaoud R, et al. Antibiotic resistance pattern of extended spectrum Beta Lactamase producing Escherichia coli isolated from patients with urinary tract infection in Morocco. Front Cell Infect Microbiol 2021; 11: 720701.
24. Singh N, Pattnaik D, Neogi DK, Jena J, Mallick B. Prevalence of ESBL in Escherichia coli isolates among ICU patients in a tertiary care hospital. J Clin Diagn Res 2016; 10: DC19-DC22.
25. Ballesteros-Monrreal MG, Arenas-Hernández MM, Enciso-Martínez Y, Martínez-de la Peña C F, Del C Rocha-Gracia R, Lozano-Zarain P, et al. Virulence and resistance determinants of uropathogenic Escherichia coli strains isolated from pregnant and non-pregnant women from two states in Mexico. Infect Drug Resist 2020; 13: 295-310.
26. Wang Y, Zhao S, Han L, Guo X, Chen M, Ni Y, et al. Drug resistance and virulence of uropathogenic Escherichia coli from Shanghai, China. J Antibiot (Tokyo) 2014; 67: 799-805.
27. Lee DS, Lee SJ, Choe HS. Community-acquired urinary tract infection by Escherichia coli in the era of antibiotic resistance. Biomed Res Int 2018; 2018: 7656752.
28. Ndzime YM, Onanga R, Kassa RFK, Bignoumba M, Nguema PPM, Gafou A, et al. Epidemiology of community origin Escherichia coli and uropathogenic strains resistant to antibiotics in Franceville, Gabon. Infect Drug Resist 2021; 14: 585-594.
29. Ventola CL. The antibiotic resistance crisis: part 1: causes and threats. P T 2015; 40: 277-283.
30. Petca RC, Negoiță S, Mareș C, Petca A, Popescu RI, Chibelean CB. Heterogeneity of antibiotics multidrug-resistance profile of uropathogens in Romanian population. Antibiotics (Basel) 2021; 10: 523.
31. Tenney J, Hudson N, Alnifaidy H, Li JTC, Fung KH. Risk factors for aquiring multidrug-resistant organisms in urinary tract infections: a systematic literature review. Saudi Pharm J 2018; 26: 678-684.
32. Boroumand M, Naghmachi M, Ghatee MA. Detection of phylogenetic groups and drug resistance genes of Escherichia coli causing urinary tract infection in southwest Iran. Jundishapur J Microbiol 2021; 14(2):e112547.
33. Sokurenko EV, Chesnokova V, Dykhuizen DE, Ofek I, Wu XR, Krogfelt KA, et al. Pathogenic adaptation of Escherichia coli by natural variation of the FimH adhesin. Proc Natl Acad Sci U S A 1998; 95: 8922-8926.
34. Sabaté M, Moreno E, Pérez T, Andreu A, Prats G. Pathogenicity island markers in commensal and uropathogenic Escherichia coli isolates. Clin Microbiol Infect 2006; 12: 880-886.
35. Chakraborty A, Saralaya V, Adhikari P, Shenoy S, Baliga S, Hegde A. Characterization of Escherichia coli phylogenetic groups associated with extraintestinal infections in South Indian population. Ann Med Health Sci Res 2015; 5: 241-246.
36. Hernández-Chiñas U, Pérez-Ramos A, Belmont-Monroy L, Chávez-Berrocal ME, González-Villalobos E, Navarro-Ocaña A, et al. Characterization of auto-agglutinating and non-typeable uropathogenic Escherichia coli strains. J Infect Dev Ctries 2019; 13: 465-472.
37. Dadi BR, Abebe T, Zhang L, Mihret A, Abebe W, Amogne W. Drug resistance and plasmid profile of uropathogenic Escherichia coli among urinary tract infection patients in Addis Abeba. J Infect Dev Ctries 2018; 12: 608-615.
38. Terlizzi ME, Gribaudo G, Maffei ME. UroPathogenic Escherichia coli (UPEC) infections: virulence factors, bladder responses, antibiotic, and non-antibiotic antimicrobial strategies. Front Microbiol 2017; 8: 1566.
39. Tabasi M, Karam M R A, Habibi M, Mostafavi E, Bouzari S. Genotypic characterization of virulence factors in Escherichia coli isolated from patients with acute cystitis, pyelonephritis and asymptomatic bacteriuria. J Clin Diagn Res 2016; 10: DC01-DC07.
40. Ghavidel M, Gholamhosseini-Moghadam T, Nourian K, Ghazvini K. Virulence factors analysis and antibiotic resistance of uropathogenic Escherichia coli isolated from patients in northeast of Iran. Iran J Microbiol 2020; 12: 223-230.
| Files | ||
| Issue | Vol 14 No 4 (2022) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v14i4.10230 | |
| Keywords | ||
| Urinary tract infections; Uropathogenic Escherichia coli; Phylogenetic groups; Serogroup; Drug resistance; Virulence factors | ||
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How to Cite
1.
Mohammed E, Hasan K, Allami M. Phylogenetic groups, serogroups and virulence factors of uropathogenic Escherichia coli isolated from patients with urinary tract infection in Baghdad, Iraq. Iran J Microbiol. 2022;14(4):445-457.
