Description of extraintestinal pathogenic Escherichia coli based on phylogenetic grouping, virulence factors, and antimicrobial susceptibility
,
Abstract
Background and Objectives: Extraintestinal pathogenic Escherichia coli (ExPEC) is a recently recognized and highly diverse pathotype of E. coli. Its significance as a pathogen has increased due to the emergence of hypervirulent and multidrug-resistant (MDR) strains. The aim of this study was to characterize ExPEC isolates from humans based on their phylogenetic group, virulence factor profile, and antimicrobial susceptibility.
Materials and Methods: The isolates were collected from patients with extraintestinal infections caused by E. coli, including urinary tract infections, bacteremia, and surgical site infections. The E. coli phylogenetic groups were determined using multiplex PCR. Additionally, the isolates were evaluated for their biofilm-forming abilities, susceptibility to antimicrobial agents, and presence of virulence genes.
Results: In this study, the isolates were classified into four phylogenetic groups: A (48.3%), B2 (25.8%), D (19.35%), and B1 (6.45%). All isolates exhibited at least one of the ten analyzed virulence factors. However, there was no direct evidence linking a specific phylogenetic group to a particular virulence factor. Nevertheless, the presence of the fimH, fyuA, ompT, traT, and kpsMTII virulence genes was correlated with the production of strong biofilms, multidrug resistance (MDR), and the production of alpha hemolysin.
Conclusion: This study provides a description of the phylogenetic groups in ExPEC and their potential association with virulence factor profiles and antimicrobial susceptibility.
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2. Sarowska J, Futoma-Koloch B, Jama-Kmiecik A, Frej-Madrzak M, Ksiazczyk M, Bugla-Ploskonska G, et al. Virulence factors, prevalence and potential transmission of extraintestinal pathogenic Escherichia coli isolated from different sources: recent reports. Gut Pathog 2019; 11: 10.
3. Kaper JB, Nataro JP, Mobley HL. Pathogenic Escherichia coli. Nat Rev Microbiol 2004; 2: 123-140.
4. Peirano G, Mulvey GL, Armstrong GD, Pitout JD. Virulence potential and adherence properties of Escherichia coli that produce CTX-M and NDM β-lactamases. J Med Microbiol 2013; 62: 525-530.
5. Clermont O, Bonacorsi S, Bingen E. Rapid and simple determination of the Escherichia coli phylogenetic group. Appl Environ Microbiol 2000; 66: 4555-4558.
6. Chaudhuri RR, Henderson IR. The evolution of the Escherichia coli phylogeny. Infect Genet Evol 2012; 12: 214-226.
7. Johnson TJ, Wannemuehler Y, Doetkott C, Johnson SJ, Rosenberger SC, Nolan LK. Identification of minimal predictors of avian pathogenic Escherichia coli virulence for use as a rapid diagnostic tool. J Clin Microbiol 2008; 46: 3987-3996.
8. Johnson JR, Johnston B, Clabots C, Kuskowski MA, Castanheira M. Escherichia coli sequence type ST131 as the major cause of serious multidrug-resistant E. coli infections in the United States. Clin Infect Dis 2010; 51: 286-294.
9. Van der Bij AK, Peirano G, Pitondo-Silva A, Pitout JD. The presence of genes encoding for different virulence factors in clonally related Escherichia coli that produce CTX-Ms. Diagn Microbiol Infect Dis 2012; 72: 297-302.
10. Cunha MPV, Saidenberg AB, Moreno AM, Ferreira AJP, Vieira MAM, Gomes TAT, et al. Pandemic extra-intestinal pathogenic Escherichia coli (ExPEC) clonal group O6-B2-ST73 as a cause of avian colibacillosis in Brazil. PLoS One 2017; 12(6): e0178970.
11. Cordoni G, Woodward MJ, Wu H, Alanazi M, Wallis T, La Ragione RM. Comparative genomics of European avian pathogenic E. coli (APEC). BMC Genomics 2016; 17: 960.
12. Baldiris-Avila R, Montes-Robledo A, Buelvas-Montes Y. Phylogenetic classification, biofilm-forming Capacity, virulence factors, and antimicrobial resistance in uropathogenic Escherichia coli (UPEC). Curr Microbiol 2020; 77: 3361-3370.
13. Gómez-Duarte OG, Arzuza O, Urbina D, Bai J, Guerra J, Montes O, et al. Detection of Escherichia coli enteropathogens by multiplex polymerase chain reaction from children's diarrheal stools in two Caribbean–Colombian cities. Foodborne Pathog Dis 2010; 7: 199-206.
14. 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.
15. Nakano M, Yamamoto S, Terai A, Ogawa O, Makino SI, Hayashi H, et al. Structural and sequence diversity of the pathogenicity island of uropathogenic Escherichia coli which encodes the USP protein. FEMS Microbiol Lett 2001; 205: 71-76.
16. Johnson TJ, Siek KS, Johnson SJ, Nolan LK. DNA sequence of a ColV plasmid and prevalence of selected plasmid-encoded virulence genes among avian Escherichia coli strains. J Bacteriol 2006; 188: 745-758.
17. Sewid AH, Hassan MN, Ammar AM, Bemis DA, Kania SA. Identification, cloning, and characterization of Staphylococcus pseudintermedius coagulase. Infect Immun 2018; 86(8): e00027-18.
18. Bokranz W, Wang X, Tschäpe H, Römling U. Expression of cellulose and curli fimbriae by Escherichia coli isolated from the gastrointestinal tract. J Med Microbiol 2005; 54: 1171-1182.
19. Montes-Robledo A, Baldiris-Avila R, Galindo JF. D-Mannoside fimH Inhibitors as non-antibiotic Aalternatives for uropathogenic Escherichia coli. Antibiotics (Basel) 2021; 10: 1072.
20. Stepanović S, Vuković D, Hola V, Di Bonaventura G, Djukić S, Ćirković I, et al. Quantification of biofilm in microtiter plates: overview of testing conditions and practical recommendations for assessment of biofilm production by staphylococci. APMIS 2007; 115: 891-899.
21. Yeh E, Pinsky BA, Banaei N, Baron EJ. Hair sheep blood, citrated or defibrinated, fulfills all requirements of blood agar for diagnostic microbiology laboratory tests. PLoS One 2009; 4(7): e6141.
22. Humphries R, Bobenchik AM, Hindler JA, Schuetz AN. Overview of changes to the clinical and laboratory standards institute performance standards for antimicrobial susceptibility testing, M100, 31st edition. J Clin Microbiol 2021; 59(12): e0021321.
23. Magiorakos A-P, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, 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.
24. Bong CW, Low KY, Chai LC, Lee CW. Prevalence and diversity of antibiotic resistant Escherichia coli from anthropogenic-impacted Larut River. Front Public Health 2022; 10: 794513.
25. Lezameta L, Gonzáles-Escalante E, Tamariz JH. Comparación de cuatro métodos fenotípicos para la detección de beta-lactamasas de espectro extendido [Comparison of four phenotypic methods to detect extended-spectrum betalactamases]. Rev Peru Med Exp Salud Publica 2010; 27: 345-351.
26. Clermont O, Gordon D, Denamur E. Guide to the various phylogenetic classification schemes for Escherichia coli and the correspondence among schemes. Microbiology (Reading) 2015; 161: 980-988.
27. Gordon DM (2013). The ecology of Escherichia coli. In Escherichia coli, Second ed. Donnenberg, M.S. (ed). Boston, MA, USA: Academic Press, pp. 3-20.
28. Ranjbar R, Nazari S, Farahani O. Phylogenetic analysis and antimicrobial resistance profiles of Escherichia coli strains isolated from UTI-suspected patients. Iran J Public Health 2020; 49: 1743-1749.
29. Pompilio A, Crocetta V, Savini V, Petrelli D, Di Nicola M, Bucco S, et al. Phylogenetic relationships, biofilm formation, motility, antibiotic resistance and extended virulence genotypes among Escherichia coli strains from women with community-onset primitive acute pyelonephritis. PLoS One 2018; 13(5): e0196260.
30. Bozcal E, Eldem V, Aydemir S, Skurnik M. The relationship between phylogenetic classification, virulence and antibiotic resistance of extraintestinal pathogenic Escherichia coli in İzmir province, Turkey. Peer J 2018; 6: e5470.
31. Ahumada-Santos YP, Báez-Flores ME, Díaz-Camacho SP, Uribe-Beltrán MJ, Eslava-Campos CA, Parra-Unda JR, et al. Association of phylogenetic distribution and presence of integrons with multidrug resistance in Escherichia coli clinical isolates from children with diarrhoea. J Infect Public Health 2020; 13: 767-772.
32. Croxen MA, Finlay BB. Molecular mechanisms of Escherichia coli pathogenicity. Nat Rev Microbiol 2010; 8: 26-38.
33. Franz E, Veenman C, Van Hoek AH, de Roda Husman A, Blaak H. Pathogenic Escherichia coli producing extended-spectrum β-lactamases isolated from surface water and wastewater. Sci Rep 2015; 5: 14372.
34. 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.
35. García V, Lestón, L, Parga A, García-Meniño I, Fernández J, Otero A, et al. Genomics, biofilm formation and infection of bladder epithelial cells in potentially uropathogenic Escherichia coli (UPEC) from animal sources and human urinary tract infections (UTIs) further support food-borne transmission. One Health 2023; 16: 100558.
36. Hancock V, Ferrieres L, Klemm P. The ferric yersiniabactin uptake receptor FyuA is required for efficient biofilm formation by urinary tract infectious Escherichia coli in human urine. Microbiology (Reading) 2008; 154: 167-175.
37. Watnick P, Kolter R. Biofilm, city of microbes. J Bacteriol 2000; 182: 2675-2679.
38. Nielsen DW, Klimavicz JS, Cavender T, Wannemuehler Y, Barbieri NL, Nolan LK, et al. The impact of media, phylogenetic classification, and E. coli pathotypes on biofilm formation in extraintestinal and commensal E. coli From humans and animals. Front Microbiol 2018; 9: 902.
39. Sauer K. The genomics and proteomics of biofilm formation. Genome Biol 2003; 4: 219.
40. Römling U. Characterization of the rdar morphotype, a multicellular behaviour in Enterobacteriaceae. Cell Mol Life Sci 2005; 62: 1234-1246.
41. Millán Y, Hernández E, Millán B, Araque M. Distribución de grupos filogenéticos y factores de virulencia en cepas de Escherichia coli uropatógena productora de β-lactamasa CTX-M-15 aisladas de pacientes de la comunidad en Mérida, Venezuela [Distribution of phylogenetic groups and virulence factors in CTX-M-15 β-lactamase-producing uropathogenic Escherichia coli strains isolated from patients in the community of Mérida, Venezuela]. Rev Argent Microbiol 2014; 46: 175-181.
42. Chen SL, Wu M, Henderson JP, Hooton TM, Hibbing ME, Hultgren SJ, et al. Genomic diversity and fitness of E. coli strains recovered from the intestinal and urinary tracts of women with recurrent urinary tract infection. Sci Transl Med 2013; 5: 184ra60.
43. 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: 445-457.
2. Sarowska J, Futoma-Koloch B, Jama-Kmiecik A, Frej-Madrzak M, Ksiazczyk M, Bugla-Ploskonska G, et al. Virulence factors, prevalence and potential transmission of extraintestinal pathogenic Escherichia coli isolated from different sources: recent reports. Gut Pathog 2019; 11: 10.
3. Kaper JB, Nataro JP, Mobley HL. Pathogenic Escherichia coli. Nat Rev Microbiol 2004; 2: 123-140.
4. Peirano G, Mulvey GL, Armstrong GD, Pitout JD. Virulence potential and adherence properties of Escherichia coli that produce CTX-M and NDM β-lactamases. J Med Microbiol 2013; 62: 525-530.
5. Clermont O, Bonacorsi S, Bingen E. Rapid and simple determination of the Escherichia coli phylogenetic group. Appl Environ Microbiol 2000; 66: 4555-4558.
6. Chaudhuri RR, Henderson IR. The evolution of the Escherichia coli phylogeny. Infect Genet Evol 2012; 12: 214-226.
7. Johnson TJ, Wannemuehler Y, Doetkott C, Johnson SJ, Rosenberger SC, Nolan LK. Identification of minimal predictors of avian pathogenic Escherichia coli virulence for use as a rapid diagnostic tool. J Clin Microbiol 2008; 46: 3987-3996.
8. Johnson JR, Johnston B, Clabots C, Kuskowski MA, Castanheira M. Escherichia coli sequence type ST131 as the major cause of serious multidrug-resistant E. coli infections in the United States. Clin Infect Dis 2010; 51: 286-294.
9. Van der Bij AK, Peirano G, Pitondo-Silva A, Pitout JD. The presence of genes encoding for different virulence factors in clonally related Escherichia coli that produce CTX-Ms. Diagn Microbiol Infect Dis 2012; 72: 297-302.
10. Cunha MPV, Saidenberg AB, Moreno AM, Ferreira AJP, Vieira MAM, Gomes TAT, et al. Pandemic extra-intestinal pathogenic Escherichia coli (ExPEC) clonal group O6-B2-ST73 as a cause of avian colibacillosis in Brazil. PLoS One 2017; 12(6): e0178970.
11. Cordoni G, Woodward MJ, Wu H, Alanazi M, Wallis T, La Ragione RM. Comparative genomics of European avian pathogenic E. coli (APEC). BMC Genomics 2016; 17: 960.
12. Baldiris-Avila R, Montes-Robledo A, Buelvas-Montes Y. Phylogenetic classification, biofilm-forming Capacity, virulence factors, and antimicrobial resistance in uropathogenic Escherichia coli (UPEC). Curr Microbiol 2020; 77: 3361-3370.
13. Gómez-Duarte OG, Arzuza O, Urbina D, Bai J, Guerra J, Montes O, et al. Detection of Escherichia coli enteropathogens by multiplex polymerase chain reaction from children's diarrheal stools in two Caribbean–Colombian cities. Foodborne Pathog Dis 2010; 7: 199-206.
14. 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.
15. Nakano M, Yamamoto S, Terai A, Ogawa O, Makino SI, Hayashi H, et al. Structural and sequence diversity of the pathogenicity island of uropathogenic Escherichia coli which encodes the USP protein. FEMS Microbiol Lett 2001; 205: 71-76.
16. Johnson TJ, Siek KS, Johnson SJ, Nolan LK. DNA sequence of a ColV plasmid and prevalence of selected plasmid-encoded virulence genes among avian Escherichia coli strains. J Bacteriol 2006; 188: 745-758.
17. Sewid AH, Hassan MN, Ammar AM, Bemis DA, Kania SA. Identification, cloning, and characterization of Staphylococcus pseudintermedius coagulase. Infect Immun 2018; 86(8): e00027-18.
18. Bokranz W, Wang X, Tschäpe H, Römling U. Expression of cellulose and curli fimbriae by Escherichia coli isolated from the gastrointestinal tract. J Med Microbiol 2005; 54: 1171-1182.
19. Montes-Robledo A, Baldiris-Avila R, Galindo JF. D-Mannoside fimH Inhibitors as non-antibiotic Aalternatives for uropathogenic Escherichia coli. Antibiotics (Basel) 2021; 10: 1072.
20. Stepanović S, Vuković D, Hola V, Di Bonaventura G, Djukić S, Ćirković I, et al. Quantification of biofilm in microtiter plates: overview of testing conditions and practical recommendations for assessment of biofilm production by staphylococci. APMIS 2007; 115: 891-899.
21. Yeh E, Pinsky BA, Banaei N, Baron EJ. Hair sheep blood, citrated or defibrinated, fulfills all requirements of blood agar for diagnostic microbiology laboratory tests. PLoS One 2009; 4(7): e6141.
22. Humphries R, Bobenchik AM, Hindler JA, Schuetz AN. Overview of changes to the clinical and laboratory standards institute performance standards for antimicrobial susceptibility testing, M100, 31st edition. J Clin Microbiol 2021; 59(12): e0021321.
23. Magiorakos A-P, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, 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.
24. Bong CW, Low KY, Chai LC, Lee CW. Prevalence and diversity of antibiotic resistant Escherichia coli from anthropogenic-impacted Larut River. Front Public Health 2022; 10: 794513.
25. Lezameta L, Gonzáles-Escalante E, Tamariz JH. Comparación de cuatro métodos fenotípicos para la detección de beta-lactamasas de espectro extendido [Comparison of four phenotypic methods to detect extended-spectrum betalactamases]. Rev Peru Med Exp Salud Publica 2010; 27: 345-351.
26. Clermont O, Gordon D, Denamur E. Guide to the various phylogenetic classification schemes for Escherichia coli and the correspondence among schemes. Microbiology (Reading) 2015; 161: 980-988.
27. Gordon DM (2013). The ecology of Escherichia coli. In Escherichia coli, Second ed. Donnenberg, M.S. (ed). Boston, MA, USA: Academic Press, pp. 3-20.
28. Ranjbar R, Nazari S, Farahani O. Phylogenetic analysis and antimicrobial resistance profiles of Escherichia coli strains isolated from UTI-suspected patients. Iran J Public Health 2020; 49: 1743-1749.
29. Pompilio A, Crocetta V, Savini V, Petrelli D, Di Nicola M, Bucco S, et al. Phylogenetic relationships, biofilm formation, motility, antibiotic resistance and extended virulence genotypes among Escherichia coli strains from women with community-onset primitive acute pyelonephritis. PLoS One 2018; 13(5): e0196260.
30. Bozcal E, Eldem V, Aydemir S, Skurnik M. The relationship between phylogenetic classification, virulence and antibiotic resistance of extraintestinal pathogenic Escherichia coli in İzmir province, Turkey. Peer J 2018; 6: e5470.
31. Ahumada-Santos YP, Báez-Flores ME, Díaz-Camacho SP, Uribe-Beltrán MJ, Eslava-Campos CA, Parra-Unda JR, et al. Association of phylogenetic distribution and presence of integrons with multidrug resistance in Escherichia coli clinical isolates from children with diarrhoea. J Infect Public Health 2020; 13: 767-772.
32. Croxen MA, Finlay BB. Molecular mechanisms of Escherichia coli pathogenicity. Nat Rev Microbiol 2010; 8: 26-38.
33. Franz E, Veenman C, Van Hoek AH, de Roda Husman A, Blaak H. Pathogenic Escherichia coli producing extended-spectrum β-lactamases isolated from surface water and wastewater. Sci Rep 2015; 5: 14372.
34. 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.
35. García V, Lestón, L, Parga A, García-Meniño I, Fernández J, Otero A, et al. Genomics, biofilm formation and infection of bladder epithelial cells in potentially uropathogenic Escherichia coli (UPEC) from animal sources and human urinary tract infections (UTIs) further support food-borne transmission. One Health 2023; 16: 100558.
36. Hancock V, Ferrieres L, Klemm P. The ferric yersiniabactin uptake receptor FyuA is required for efficient biofilm formation by urinary tract infectious Escherichia coli in human urine. Microbiology (Reading) 2008; 154: 167-175.
37. Watnick P, Kolter R. Biofilm, city of microbes. J Bacteriol 2000; 182: 2675-2679.
38. Nielsen DW, Klimavicz JS, Cavender T, Wannemuehler Y, Barbieri NL, Nolan LK, et al. The impact of media, phylogenetic classification, and E. coli pathotypes on biofilm formation in extraintestinal and commensal E. coli From humans and animals. Front Microbiol 2018; 9: 902.
39. Sauer K. The genomics and proteomics of biofilm formation. Genome Biol 2003; 4: 219.
40. Römling U. Characterization of the rdar morphotype, a multicellular behaviour in Enterobacteriaceae. Cell Mol Life Sci 2005; 62: 1234-1246.
41. Millán Y, Hernández E, Millán B, Araque M. Distribución de grupos filogenéticos y factores de virulencia en cepas de Escherichia coli uropatógena productora de β-lactamasa CTX-M-15 aisladas de pacientes de la comunidad en Mérida, Venezuela [Distribution of phylogenetic groups and virulence factors in CTX-M-15 β-lactamase-producing uropathogenic Escherichia coli strains isolated from patients in the community of Mérida, Venezuela]. Rev Argent Microbiol 2014; 46: 175-181.
42. Chen SL, Wu M, Henderson JP, Hooton TM, Hibbing ME, Hultgren SJ, et al. Genomic diversity and fitness of E. coli strains recovered from the intestinal and urinary tracts of women with recurrent urinary tract infection. Sci Transl Med 2013; 5: 184ra60.
43. 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: 445-457.
| Files | ||
| Issue | Vol 15 No 4 (2023) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v15i4.13504 | |
| Keywords | ||
| Escherichia coli; Virulence factor; Antibiotic resistance; Phylogeny; Biofilm | ||
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How to Cite
1.
Montes-Robledo A, Buelvas-Montes Y, Baldiris-Avila R. Description of extraintestinal pathogenic Escherichia coli based on phylogenetic grouping, virulence factors, and antimicrobial susceptibility. Iran J Microbiol. 2023;15(4):503-512.
