The relationship between phylogenetic groups and antibiotic susceptibility patterns of Escherichia coli strains isolated from feces and urine of patients with acute or recurrent urinary tract infection
-
Hossein Norouzian
,
Mohammad Katouli
,
Nader Shahrokhi
,
Shahram Sabeti
,
Mohammad Pooya
,
Saeid Bouzari
Abstract
Background and Objectives: B2 and D have been mentioned as the most common phylogenetic groups among uropathogenic Escherichia coli. However, there is still controversy about the importance of these phylo-groups. This study was conducted to investigate the probable relation between these groups and antibiotic resistance patterns of E. coli isolates derived from urine and feces of the patients with acute or recurrent UTI.
Materials and Methods: 10 isolates were recovered from urine and feces samples of patients with different phases of UTI in whom E. coli was causative pathogen. Biochemical fingerprinting was performed to classify the isolates and select their appropriate representatives. Phylogenetic grouping was performed using multiplex PCR, and antibiotic resistance was determined by disk diffusion method.
Results: Five-hundred-sixty E. coli isolates were derived from 56 UTI patients (27 acute, 29 recurrent). Among them, 261 isolates were selected using biochemical fingerprinting. All the isolates were sensitive to imipenem and nitrofurantoin. Compared to other phylo-groups, the isolates in group D showed considerably different frequencies in acute vs. recurrent phase of UTI, in urine vs. stool samples, in males vs. females, and in- vs. out-patients. They were more resistant to the antibiotics (except norfloxacin), and in contrast to others, this was seen more in acute UTI, especially in urine samples. Multi-drug resistance pattern was also meaningfully higher in group D.
Conclusion: Although phylo-groups B2 and D of E. coli bacteria are more responsible for UTI, group D isolates seem to be more resistant and probably more virulent, even than the ones from group B2.
1. Hooton TM. Recurrent urinary tract infection in women. Int J Antimicrob Agents 2001;17:259-268.
2. Foxman B. The epidemiology of urinary tract infection. Nat Rev Urol 2010;7:653-660.
3. Foxman B. Recurring urinary tract infection: incidence and risk factors. Am J Public Health 1990;80:331-333.
4. Flores-Mireles AL, Walker JN, Caparon M, Hultgren SJ. Urinary tract infections: epidemiology, mechanisms of infection and treatment options. Nat Rev Microbiol 2015;13:269-284.
5. Kühn I. Biochemical fingerprinting of Escherichia coli: a simple method for epidemiological investigations. J Microbiol Methods 1985;3:159-170.
6. Möllby R, Kühn I, Katouli M. Computerised biochemical fingerprinting a new tool for typing of bacteria. Rev Med Microbiol 1993;4:231-241.
7. Katouli M, Kühn I, Wollin R, Möllby R. Evaluation of the PhP system for biochemical-fingerprint typing of strains of Salmonella of serotype Typhimurium. J Med Microbiol 1992;37:245-251.
8. Kühn I, Burman LG, Haeggman S, Tullus K, Murray BE. Biochemical fingerprinting compared with ribotyping and pulsed-field gel electrophoresis of DNA for epidemiological typing of enterococci. J Clin Microbiol 1995;33:2812-2817.
9. Tullus K, Kühn I, Källenius G, Wrangsell G, Ørskov F, Ørskov I, et al. Fecal colonization with pyelonephritogenic Escherichia coli in neonates as a risk factor for pyelonephritis. Eur J Clin Microbiol 1986;5:643-648.
10. Clermont O, Bonacorsi S, Bingen E. Rapid and simple determination of the Escherichia coli phylogenetic group. Appl Environ Microbiol 2000;66:4555-4558.
11. Johnson JR, Delavari P, Kuskowski M, Stell AL. Phylogenetic distribution of extraintestinal virulence-associated traits in Escherichia coli. J Infect Dis 2001;183:78-88.
12. Johnson JR, Stell AL. Extended virulence genotypes of Escherichia coli strains from patients with urosepsis in relation to phylogeny and host compromise. J Infect Dis 2000;181:261-272.
13. Taheri M, Saleh M, Nemati AH, Ariana M, Shojaei E, Mardani M, et al. Antibiotic resistance pattern and phylogenetic groups of the Uropathogenic Escherichia coli isolates recovered from the urinary catheters of the hospitalized patients. JoMMID 2016;4:76-82.
14. Zowawi HM, Harris PN, Roberts MJ, Tambyah PA, Schembri MA, Pezzani MD, et al. The emerging threat of multidrug-resistant Gram-negative bacteria in urology. Nat Rev Urol 2015;12:570-584.
15. Magiorakos AP, Srinivasan A, Carey R, Carmeli Y, Falagas M, Giske C, et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect 2012;18:268-281.
16. Kõljalg S, Truusalu K, Stsepetova J, Pai K, Vainumäe I, Sepp E, et al. The Escherichia coli phylogenetic group B2 with integrons prevails in childhood recurrent urinary tract infections. APMIS 2013;122:452-458.
17. Anger J, Lee U, Ackerman AL, Chou R, Chughtai B, Clemens JQ, et al. Recurrent Uncomplicated Urinary Tract Infections in Women: AUA/CUA/SUFU Guideline. J Urol 2019;202:282-289.
18. Foxman B, Manning SD, Tallman P, Bauer R, Zhang L, Koopman JS, et al. Uropathogenic Escherichia coli are more likely than commensal E. coli to be shared between heterosexual sex partners. Am J Epidemiol 2002;156:1133-1140.
19. Pérez-Pérez FJ, Hanson ND. Detection of plasmid-mediated AmpC β-lactamase genes in clinical isolates by using multiplex PCR. J Clin Microbiol 2002;40:2153-2162.
20. Duriez P, Clermont O, Bonacorsi S, Bingen E, Chaventré A, Elion J, et al. Commensal Escherichia coli isolates are phylogenetically distributed among geographically distinct human populations. Microbiology 2001;147:1671-1676.
21. Picard B, Garcia JS, Gouriou S, Duriez P, Brahimi N, Bingen E, et al. The link between phylogeny and virulence in Escherichia coli extraintestinal infection. Infect Immun 1999;67:546-553.
22. Luo Y, Ma Y, Zhao Q, Wang L, Guo L, Ye L, et al. Similarity and divergence of phylogenies, antimicrobial susceptibilities, and virulence factor profiles of Escherichia coli isolates causing recurrent urinary tract infections that persist or result from reinfection. J Clin Microbiol 2012;50:4002-4007.
23. Staji H, Rassouli M, Jourablou S. Comparative virulotyping and phylogenomics of Escherichia coli isolates from urine samples of men and women suffering urinary tract infections. Iran J Basic Med Sci 2019;22:211-214.
24. Matta R, Hallit S, Hallit R, Bawab W, Rogues A-M, Salameh P. Epidemiology and microbiological profile comparison between community and hospital acquired infections: a multicenter retrospective study in Lebanon. J Infect Public Health 2018;11:405-411.
25. Manges AR, Johnson JR, Foxman B, O'Bryan TT, Fullerton KE, Riley LW. Widespread distribution of urinary tract infections caused by a multidrug-resistant Escherichia coli clonal group. N Engl J Med 2001;345:1007-1013.
26. López-Banda DA, Carrillo-Casas EM, Leyva-Leyva M, Orozco-Hoyuela G, Manjarrez-Hernández ÁH, Arroyo-Escalante S, et al. Identification of virulence factors genes in Escherichia coli isolates from women with urinary tract infection in Mexico. Biomed Res Int 2014;2014: 959206.
27. 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.
28. Lee DS, Lee S-J, Choe H-S. Community-acquired urinary tract infection by Escherichia coli in the era of antibiotic resistance. Biomed Res Int 2018;2018:7656752.
29. Andrade SS, Sader HS, Jones RN, Pereira AS, Pignatari AC, Gales AC. Increased resistance to first-line agents among bacterial pathogens isolated from urinary tract infections in Latin America: time for local guidelines? Mem Inst Oswaldo Cruz 2006;101:741-748.
30. Johnson JR, Kuskowski MA, Owens K, Gajewski A, Winokur PL. Phylogenetic origin and virulence genotype in relation to resistance to fluoroquinolones and/or extended-spectrum cephalosporins and cephamycins among Escherichia coli isolates from animals and humans. J Infect Dis 2003;188:759-768.
31. Bashir S, Sarwar Y, Ali A, Mohsin M, Saeed MA, Tariq A, et al. Multiple drug resistance patterns in various phylogenetic groups of uropathogenic E. coli isolated from Faisalabad region of Pakistan. Braz J Microbiol 2011;42:1278-1283.
32. 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.
33. Iranpour D, Hassanpour M, Ansari H, Tajbakhsh S, Khamisipour G, Najafi A. Phylogenetic groups of Escherichia coli strains from patients with urinary tract infection in Iran based on the new Clermont phylotyping method. Biomed Res Int 2015;2015:846219.
34. MuKherjee M, BaSu S, MuKherjee SK, MajuMder M. Multidrug-resistance and extended spectrum beta-lactamase production in uropathogenic E. Coli which were isolated from hospitalized patients in Kolkata, India. Journal of clinical and diagnostic research. J Clin Diagn Res 2013;7:449-453.
35. Foxman B, Zhang L, Tallman P, Palin K, Rode C, Bloch C, et al. Virulence characteristics of Escherichia coli causing first urinary tract infection predict risk of second infection. J Infect Dis 1995;172:1536-1541.
2. Foxman B. The epidemiology of urinary tract infection. Nat Rev Urol 2010;7:653-660.
3. Foxman B. Recurring urinary tract infection: incidence and risk factors. Am J Public Health 1990;80:331-333.
4. Flores-Mireles AL, Walker JN, Caparon M, Hultgren SJ. Urinary tract infections: epidemiology, mechanisms of infection and treatment options. Nat Rev Microbiol 2015;13:269-284.
5. Kühn I. Biochemical fingerprinting of Escherichia coli: a simple method for epidemiological investigations. J Microbiol Methods 1985;3:159-170.
6. Möllby R, Kühn I, Katouli M. Computerised biochemical fingerprinting a new tool for typing of bacteria. Rev Med Microbiol 1993;4:231-241.
7. Katouli M, Kühn I, Wollin R, Möllby R. Evaluation of the PhP system for biochemical-fingerprint typing of strains of Salmonella of serotype Typhimurium. J Med Microbiol 1992;37:245-251.
8. Kühn I, Burman LG, Haeggman S, Tullus K, Murray BE. Biochemical fingerprinting compared with ribotyping and pulsed-field gel electrophoresis of DNA for epidemiological typing of enterococci. J Clin Microbiol 1995;33:2812-2817.
9. Tullus K, Kühn I, Källenius G, Wrangsell G, Ørskov F, Ørskov I, et al. Fecal colonization with pyelonephritogenic Escherichia coli in neonates as a risk factor for pyelonephritis. Eur J Clin Microbiol 1986;5:643-648.
10. Clermont O, Bonacorsi S, Bingen E. Rapid and simple determination of the Escherichia coli phylogenetic group. Appl Environ Microbiol 2000;66:4555-4558.
11. Johnson JR, Delavari P, Kuskowski M, Stell AL. Phylogenetic distribution of extraintestinal virulence-associated traits in Escherichia coli. J Infect Dis 2001;183:78-88.
12. Johnson JR, Stell AL. Extended virulence genotypes of Escherichia coli strains from patients with urosepsis in relation to phylogeny and host compromise. J Infect Dis 2000;181:261-272.
13. Taheri M, Saleh M, Nemati AH, Ariana M, Shojaei E, Mardani M, et al. Antibiotic resistance pattern and phylogenetic groups of the Uropathogenic Escherichia coli isolates recovered from the urinary catheters of the hospitalized patients. JoMMID 2016;4:76-82.
14. Zowawi HM, Harris PN, Roberts MJ, Tambyah PA, Schembri MA, Pezzani MD, et al. The emerging threat of multidrug-resistant Gram-negative bacteria in urology. Nat Rev Urol 2015;12:570-584.
15. Magiorakos AP, Srinivasan A, Carey R, Carmeli Y, Falagas M, Giske C, et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect 2012;18:268-281.
16. Kõljalg S, Truusalu K, Stsepetova J, Pai K, Vainumäe I, Sepp E, et al. The Escherichia coli phylogenetic group B2 with integrons prevails in childhood recurrent urinary tract infections. APMIS 2013;122:452-458.
17. Anger J, Lee U, Ackerman AL, Chou R, Chughtai B, Clemens JQ, et al. Recurrent Uncomplicated Urinary Tract Infections in Women: AUA/CUA/SUFU Guideline. J Urol 2019;202:282-289.
18. Foxman B, Manning SD, Tallman P, Bauer R, Zhang L, Koopman JS, et al. Uropathogenic Escherichia coli are more likely than commensal E. coli to be shared between heterosexual sex partners. Am J Epidemiol 2002;156:1133-1140.
19. Pérez-Pérez FJ, Hanson ND. Detection of plasmid-mediated AmpC β-lactamase genes in clinical isolates by using multiplex PCR. J Clin Microbiol 2002;40:2153-2162.
20. Duriez P, Clermont O, Bonacorsi S, Bingen E, Chaventré A, Elion J, et al. Commensal Escherichia coli isolates are phylogenetically distributed among geographically distinct human populations. Microbiology 2001;147:1671-1676.
21. Picard B, Garcia JS, Gouriou S, Duriez P, Brahimi N, Bingen E, et al. The link between phylogeny and virulence in Escherichia coli extraintestinal infection. Infect Immun 1999;67:546-553.
22. Luo Y, Ma Y, Zhao Q, Wang L, Guo L, Ye L, et al. Similarity and divergence of phylogenies, antimicrobial susceptibilities, and virulence factor profiles of Escherichia coli isolates causing recurrent urinary tract infections that persist or result from reinfection. J Clin Microbiol 2012;50:4002-4007.
23. Staji H, Rassouli M, Jourablou S. Comparative virulotyping and phylogenomics of Escherichia coli isolates from urine samples of men and women suffering urinary tract infections. Iran J Basic Med Sci 2019;22:211-214.
24. Matta R, Hallit S, Hallit R, Bawab W, Rogues A-M, Salameh P. Epidemiology and microbiological profile comparison between community and hospital acquired infections: a multicenter retrospective study in Lebanon. J Infect Public Health 2018;11:405-411.
25. Manges AR, Johnson JR, Foxman B, O'Bryan TT, Fullerton KE, Riley LW. Widespread distribution of urinary tract infections caused by a multidrug-resistant Escherichia coli clonal group. N Engl J Med 2001;345:1007-1013.
26. López-Banda DA, Carrillo-Casas EM, Leyva-Leyva M, Orozco-Hoyuela G, Manjarrez-Hernández ÁH, Arroyo-Escalante S, et al. Identification of virulence factors genes in Escherichia coli isolates from women with urinary tract infection in Mexico. Biomed Res Int 2014;2014: 959206.
27. 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.
28. Lee DS, Lee S-J, Choe H-S. Community-acquired urinary tract infection by Escherichia coli in the era of antibiotic resistance. Biomed Res Int 2018;2018:7656752.
29. Andrade SS, Sader HS, Jones RN, Pereira AS, Pignatari AC, Gales AC. Increased resistance to first-line agents among bacterial pathogens isolated from urinary tract infections in Latin America: time for local guidelines? Mem Inst Oswaldo Cruz 2006;101:741-748.
30. Johnson JR, Kuskowski MA, Owens K, Gajewski A, Winokur PL. Phylogenetic origin and virulence genotype in relation to resistance to fluoroquinolones and/or extended-spectrum cephalosporins and cephamycins among Escherichia coli isolates from animals and humans. J Infect Dis 2003;188:759-768.
31. Bashir S, Sarwar Y, Ali A, Mohsin M, Saeed MA, Tariq A, et al. Multiple drug resistance patterns in various phylogenetic groups of uropathogenic E. coli isolated from Faisalabad region of Pakistan. Braz J Microbiol 2011;42:1278-1283.
32. 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.
33. Iranpour D, Hassanpour M, Ansari H, Tajbakhsh S, Khamisipour G, Najafi A. Phylogenetic groups of Escherichia coli strains from patients with urinary tract infection in Iran based on the new Clermont phylotyping method. Biomed Res Int 2015;2015:846219.
34. MuKherjee M, BaSu S, MuKherjee SK, MajuMder M. Multidrug-resistance and extended spectrum beta-lactamase production in uropathogenic E. Coli which were isolated from hospitalized patients in Kolkata, India. Journal of clinical and diagnostic research. J Clin Diagn Res 2013;7:449-453.
35. Foxman B, Zhang L, Tallman P, Palin K, Rode C, Bloch C, et al. Virulence characteristics of Escherichia coli causing first urinary tract infection predict risk of second infection. J Infect Dis 1995;172:1536-1541.
| Files | ||
| Issue | Vol 11 No 6 (2019) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v11i6.2219 | |
| Keywords | ||
| Uropathogenic Escherichia coli; Acute urinary tract infection; Recurrent urinary tract infection; Antibiotic resistance; Phylogenetic groups | ||
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How to Cite
1.
Norouzian H, Katouli M, Shahrokhi N, Sabeti S, Pooya M, Bouzari S. The relationship between phylogenetic groups and antibiotic susceptibility patterns of Escherichia coli strains isolated from feces and urine of patients with acute or recurrent urinary tract infection. Iran J Microbiol. 2020;11(6):478-487.
