Phylogenetic Group/Subgroups Distributions, Virulence Factors, and Antimicrobial Susceptibility of Escherichia coli Strains from Urinary Tract Infections in Hatay

Ebru Şebnem Yılmaz Özkan Aslantaş About the authors

Abstract

INTRODUCTION:

Nosocomial and community acquired urinary tract infections (UTIs) are one of the most encountered infections in the world.

METHODS:

This study aimed to determine the antibiotic susceptibility, phylogeny, and virulence genes of 153 Escherichia coli strains isolated from UTIs. Antimicrobial susceptibility of the isolates to different classes of antimicrobials was determined by the VITEK-2 automated system. Presence of virulence genes and phylogenetic groups were investigated by PCR.

RESULTS:

Regarding susceptibility to antimicrobials, ampicillin resistance was most abundant (67.3%), followed by amoxicillin-clavulanic acid (50.9%); least abundant was resistance to amikacin (1.3%) and nitrofurantoin (1.3%). Multi drug resistance (MDR) was observed in 34.6% of the isolates, and all isolates were found to be susceptible to imipenem, meropenem and fosfomycine. The majority of the isolates belonged to the phylogenetic group B23 (35.9%), followed by A1 (20.9%), D1 (18.9%), D2 (12.4%), A0 (%5.9), B1 (3.9%) and B2 (1.9%). Among E. coli strains examined, 49% had iucD, 32.7% papE-F, 26.1% papC, 15% cnf2, 11.1% sfa, 7.8% cnf1, 1.3% afaE, 1.3% afaD, 1.3% hlyA, 0.7% f17a-A, 0.7% clpG and 0.7% eaeA genes.

CONCLUSIONS

Our research demonstrated that virulence factors were distributed among different phylogroup/subgroups, which play a role in UTIs pathogenesis in humans. For this reason, complex and detailed studies are required to determine the relationship between virulence factors and specific E. coli strains that cause UTIs in humans.

Keywords:
Urinary Tract Infections; Virulence genes; Phylogenetic group; Antimicrobial resistance

INTRODUCTION

Urinary tract infections (UTIs) are one of the most common infections, affecting both outpatients and inpatients worldwide11. Paniagua-Contreras GL, Monroy-Perez E, Rodriguez-Moctezuma JR, Dominguez-Trejo P, Vaca-Paniagua F, Vaca S. Virulence factors, antibiotic resistancephenotypes and O-serogroups of Escherichia coli strains isolated from community acquired urinary tract infection patients in Mexico. J Microbiol Immunol Infect. 2015;50(4):478-85.. Uropathogenic Escherichia coli (UPEC), classified as Extraintestinal pathogenic E. coli (ExPEC), are one of the most predominant causes of UTIs22. Yun KW, Kim HK, Park HK, Kim W, Lim IS. Virulence factors of uropathogenic Escherichia coli of urinary tract infections and asymptomatic bacteriuria in children. J Microbiol Immunol Infect . 2014;47(6):455-61.. UPEC strains have several virulence factors which play an important role in the pathogenesis of infections. These virulence factors include both structural (fimbriae, pili, curli, flagella) and secreted (toxins, iron-acquisition) systems33. 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., are related to colonization and durability of bacteria in the urinary system44. Giray B, Uçar FB, Aydemir SS. Characterization of uropathogenic Escherichia coli strains obtained from urology outpatient clinic of Ege medical faculty in İzmir. Turk J Med Sci. 2012;42(1):1328-37.. In addition, it has been shown that E. coli strains causing UTIs have a higher prevalence rate of virulence genes than commensal E. coli strains55. Forsyth VS, Armbruster CE, Smith SN, Pirani A, Springman AC, Walters MS, et al. Rapid growth of uropathogenic Escherichia coli during human urinary tract infection. MBio. 2018;9(2):1-13..

Based on three genetic marker, including chuA, yjaA and DNA fragment TSPE4.C2, E. coli strains were mainly divided into four phylogenetic groups (A, B1, B2 and D) by Clermont et al. (2000)66. Clermont O, Bonacorsi S, Bingen E. Rapid and simple determination of the Escherichia coli phylogenetic group. Appl Environ Microbiol. 2000;66(10):4555-8.. Escobar-Páramo et al. (2004) further divided these phylogenetic groups into subgroups according to presence or absence of the chuA, yjaA genes and the DNA fragment TSPE4.C2 including A0, A1, B1, B2, B23, D1, D277. Escobar-Páramo P, Grenet K, Le Menac'h A, Rode L, Salgado E, Amorin C, et al. Large-scale population structure of human commensal Escherichia coli isolates. Appl Environ Microbiol . 2004;70(9):5698-700.. Previous phylogenetic analysis revealed that ExPEC strains causing UTIs mainly belonged to phylogenetic groups B2 or D, but commensal strains predominantly belonged to phylogenetic groups B1 or A44. Giray B, Uçar FB, Aydemir SS. Characterization of uropathogenic Escherichia coli strains obtained from urology outpatient clinic of Ege medical faculty in İzmir. Turk J Med Sci. 2012;42(1):1328-37.,88. Lee JH, Subhadra B, Son YJ, Kim DH, Park HS, Kim JM, et al. Phylogenetic group distributions, virulence factors andantimicrobial resistance properties of uropathogenic Escherichia coli strains isolated from patients with urinary tract infections in South Korea. Lett Appl Microbiol. 2015;62(1):84-90.. Phylogenetic grouping of E. coli isolates is of importance not only for understanding of E. coli populations, but also elucidating the relationship between strains and disease.

As observed in other bacterial pathogens, increasing antimicrobial resistance in ExPEC strains poses a serious public health threat by decreasing available treatment options for UTIs. Therefore, continuous surveillance of ExPEC strains for antimicrobial susceptibility may provide useful information that will assist physicians in administering effective UTI treatment99. Aghemwenhio IS, Timilehin AA, Alpheus GA. Susceptibility of beta-haemolytic Escherichia coli to commonly used antibiotics in selected hospitals in Delta State, Southern Nigeria. Arc Clin Microbiol. 2017;8(2):36..

Previously, there have been a few studies featuring virulence properties, antibiotic resistance, and its relationship with phylogenetic groups among E. coli associated with UTIs in Turkey1010. Giray B, Ucar F, Aydemir S. Genotypic analysis of Escherichia coli strains that cause urosepsis in the Aegean region. Turk J Med Sci . 2016;46(5):1518-27.

11. 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.

12. Paykoc EI, Turkyilmaz S. Investigation of P fimbriae presence in Escherichia coli strains isolated from urine samples in human and their antibacterial resistance. Jundishapur J Microbiol. 2018;11(9):e66119.
-1313. 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. Rev Soc Bras Med Trop. 2019;52:e20180499.. Therefore, the main objective of this study was to determine the antimicrobial susceptibility, phylogeny, and virulence genes of E. coli isolated from patients admitted to Hatay State Hospital with UTI complaint.

METHODS

E. coli strains were isolated from urine samples collected from patients admitted to Antakya State Hospital with complaint of UTI between January and June 2014. Isolates were included in the study when a pure culture containing > 105 cfu/ml was acquired. The isolates were identified with conventional biochemical tests1414. Procop G, Church D, Hall G, Janda W, Koneman E, Schrekenberger P, et al. Koneman’s color atlas and textbook of diagnostic microbiology.7th ed. Lippincott Williams and Wilkins: Philadelphia; 2017. 360-6 p. (Gram staining, oxidase, IMVIC), and confirmed by polymerase chain reaction (PCR) targeting E. coli specific 16S rRNA1515. Wang G, Clark CG, Rodgers FG. Detection in Escherichia coli of the genes encoding the major virulence factors, the genes defining the O157:H7 serotype, and components of the type 2 Shiga toxin family by multiplex PCR. J of Clinical Microbiology. 2002;40(10):3613-19..

Antimicrobial susceptibility of the isolates were performed using an automated method (VITEK®2 BioMérieux). Susceptibility to 17 antimicrobials including ampicillin, amikacin, amoxycillin-clavulanic acid, cefazolin, cefepime, cefoxitin, ceftriaxone, cefuroxime, ciprofloxacin, fosfomycin, gentamicin, imipenem, meropenem, nitrofurantoin, norfloxacin, trimethoprim-sulfamethoxazole and piperacillin-tazobactam was tested using a Gram Negative Susceptibility card (AST-N325). The isolates showing resistance to three or more antimicrobials from different classes of antimicrobials were categorized as multi drug resistant (MDR).

Bacterial genomic DNA was acquired by boil extraction method1616. Ahmed AM, Motoi Y, Sato M, Maruyama A, Watanabe H, Fukumoto Y, et al. Zoo animals as reservoirs of gram-negative bacteria harboring integrons and antimicrobial resistance genes. Appl Environ Microbiol . 2007;73(20):6686-90.. Phylogenetic grouping of the isolates was determined using multiplex PCR66. Clermont O, Bonacorsi S, Bingen E. Rapid and simple determination of the Escherichia coli phylogenetic group. Appl Environ Microbiol. 2000;66(10):4555-8.. The identification of phylogenetic groups and subgroups (A0, A1, B1, B2, B23, D1, D2) were determined based on presence or absence of the chuA, yjaA genes and the DNA fragment TspE4-C2 as previously described by Escobar-Páramo et al77. Escobar-Páramo P, Grenet K, Le Menac'h A, Rode L, Salgado E, Amorin C, et al. Large-scale population structure of human commensal Escherichia coli isolates. Appl Environ Microbiol . 2004;70(9):5698-700..

The frequency of virulence genes (papC, papE-F, sfa/focDE, cnf1, iucD, hlyA, afa D-8, afa E-8, clpG, cnf2, f17A, f17a-A, f17b-A, f17c-A, f17d-A, stx1, stx2, and eaeA) were investigated using PCR protocols1515. Wang G, Clark CG, Rodgers FG. Detection in Escherichia coli of the genes encoding the major virulence factors, the genes defining the O157:H7 serotype, and components of the type 2 Shiga toxin family by multiplex PCR. J of Clinical Microbiology. 2002;40(10):3613-19.,1717. Yamamoto S, Tsukamoto T, Terai A, Kurazono H, Takeda Y, Yoshida O. Distrubiton of virulence factors in E. coli isolated from urine of cystitis patients. Microbiol Immunol. 1995; 39(6):401-4.

18. Bertin Y, Martin C, Oswald E, Girardeau JP. Rapid and specific detection of F17-related pili and adhesin genes in diarrheic and septicemic Escherichia coli strains by multiplex PCR. J Clin Microbiol. 1996;34(12):2921-8.

19. Bertin Y, Martin C, Girardeau JP, Pohl P, Contrepois M. Association of genes encoding P fimbriae, CS31A antigen and EAST 1 toxin among CNF1-producing Escherichia coli strains from cattle with septicemia and diarrhea. FEMS Microbiol Lett. 1998;162(2):235-9.

20. Lalioui L, Jouve M, Gounon P, Le Bouguenec C. Molecular cloning and characterization of the afa7 and afa8 gene clusters encoding afimbrial adhesins in Escherichia coli strains associated with diarrhea or septicemia in calves. Infect Immun. 1999;67(10):5048-59.
-2121. Kaipainen T, Pohjanvirta T, Shpigel NY, Shwimmer A, Pyörälä S, Pelkonen S. Virulence factors of Escherichia coli isolated from bovine clinical mastitis. Vet Microbiol. 2002;85(1):37-46..

Statistical differences among phylogenetic groups/subgroups, virulence genes, and antimicrobial susceptibility results were determined using Pearson’s chi-square test. SPSS 14.01 was used for statistical analysis. In all statistical analyses a level of significance of 0.05 was adopted.

RESULTS

A total of 153 strains isolated from patient urine specimens were identified as E. coli based on standard biochemical tests and PCR amplification of the targeted 16S rRNA (Figure 1).

Antimicrobial susceptibility testing revealed that all isolates were susceptible to imipenem, meropenem and fosfomycine. Various rates of resistance to ampicillin (67.3%, n=103), amoxicillin-clavulanic acid (50.9%; n=78), cefazolin (45.1%, n=69), trimethoprim-sulfamethoxazole (45.1%, n=69), cefuroxime (38.65%, n=59), ceftriaxone (36.6%, n=56), ciprofloxacin (35.9%, n=55), cefepime (35.9%, n=55), cefoxitin (5.2%, n=8), norfloxacin (32.7%, n=50), gentamicin (20.9%, n=36), tazobactam-ticarbenicillin (19.6%; n=30), amikacin (1.3%, n=2) and nitrofurantoin (1.3%, n=2) were observed (Figure 2). MDR was observed in 34.6% (n=53) of the isolates. Forty (26.1%) isolates were found to be susceptible to all antimicrobials tested. There were no statistically significant differences among MDR, non-MDR, and susceptible isolates among phylogenetic groups/subgroups (P>0.672).

Phylogenetic grouping and subgrouping was determined as follows: 55 (35.9%) isolates belonged to group B23, 32 (20.9%) belonged to group A1, 29 (18.9%) belonged to D1, 19 (12.4%) belonged to D2, 9 (5.9 %) belonged to A0, 6 (3.9 % ) belonged to B1, and 3 (1.9 %) belonged to B2 (Figure 3).

FIGURE 1:
PCR amplification of E. coli specific 16S rRNA gene (401 bp).

FIGURE 2:
Antimicrobial resistance rates of E. coli isolates. AMP: Ampicillin; AMC: Amoxycillin-clavulanic acid; CFZ: Cefazolin; SXT: Trimethoprim-sulfamethoxazole; CXM: Cefuroxime; CRO: Ceftriaxone; CIP: Ciprofloxacin; FEB: Cefepime; NOR: Norfl oxacin; CN: Gentamicin; TPZ: Piperacillin-tazobactam; FOX: Cefoxitin; AK: Amikacin; NIT: Nitrofurantoin; FF: Fosfomycin; IMP: Imipenem; MEM: Meropenem.

FIGURE 3:
Phylogenetic groups determined among E. coli isolates.

Of the 153 E. coli isolates, 109 (71.2%) isolates carried at least one virulence gene. Distribution of virulence genes was detected as iucD (49%, n=75), papE-F (32.7%, n=50), papC (26.1%, n=40), cnf2 (15%, n=23), sfa (11.1%, n=17), cnf1 (7.8%, n=12), afaE (1.3%, n=2), afaD (1.3%, n=2), hlyA (1.3%, n=2), f17a-A (0.7%, n=1), clpG (0.7%, n=1) and eaeA (0.7%, n=1), respectively. In addition, 26 different virulence gene profiles were observed among the isolates. Distribution of virulence gene profiles based on phylogenetic groups/subgroups among the isolates were given in Table 1. Statistically significant differences were observed between the phylogenetic groups and the isolates with and without the virulence gene (P<0.001).

TABLE 1:
Distribution of virulence gene profiles according to phylogenetic group/subgroups among E. coli isolates.

DISCUSSION

Determination of antimicrobial resistance and virulence properties of E. coli strains isolated from UTIs are of importance, especially in hospitalized patients, allowing physicians to provide alternative treatment options, reducing the risk of complications, and optimizing ongoing infection control programs99. Aghemwenhio IS, Timilehin AA, Alpheus GA. Susceptibility of beta-haemolytic Escherichia coli to commonly used antibiotics in selected hospitals in Delta State, Southern Nigeria. Arc Clin Microbiol. 2017;8(2):36.. Because UTIs are often treated empirically by physicians, it is therefore necessary to understand the epidemiological data related to agents causing infection in order to improve patient outcomes2222. Flores-Mireles AL, Walker JN, Caparon M, Hultgren SJ. Urinary tract infections: epidemiology, mechanisms of infection and treatment options. Nat Rev Microbiol. 2015;13(5):269-284..

Increased antimicrobial resistance rates, particularly for beta-lactams, sulfamethoxazole-trimethoprim, third generation cephalosporins, and fluoroquinolones, has led to challenges in clinical practice2323. Chiu CC, Lin TC, Wu RX, Yang YS, Hsiao PJ, Lee Y, et al. Etiologies of community-onset urinary tract infections requiring hospitalization and antimicrobial susceptibilities of causative microorganisms. J Microbiol Immunol Infect . 2017;50(6):879-85.. In this study, nearly half of the isolates were resistant to the majority of the tested antimicrobials, with 34.6% of the strains demonstrating MDR, which is in agreement with previous studies conducted in different regions of Turkey1212. Paykoc EI, Turkyilmaz S. Investigation of P fimbriae presence in Escherichia coli strains isolated from urine samples in human and their antibacterial resistance. Jundishapur J Microbiol. 2018;11(9):e66119.,2424. Yılmaz N, Ağuş N, Bayram A, Şamlıoğlu P, Şirin MC, Derici YK and Hancı SY. Antimicrobial susceptibilities of Escherichia coli isolates as agents of community-acquired urinary tract infection (2008-2014). Turk J Urol. 2016;42(1):32-6.. In accordance with the results of the study, 67.3%, 50.9%, 45.1%, 45.1%, 38.7%, 36.6%, 35.9%, 35.9%, and 32.7% were resistant to ampicillin, amoxicillin-clavulanic acid, cefazolin, trimethoprim-sulfamethoxazole, cefuroxime, ceftriaxone, ciprofloxacin, cefepime, and norfloxacin, respectively, which are the first-line therapeutic agents used for UTI treatment2323. Chiu CC, Lin TC, Wu RX, Yang YS, Hsiao PJ, Lee Y, et al. Etiologies of community-onset urinary tract infections requiring hospitalization and antimicrobial susceptibilities of causative microorganisms. J Microbiol Immunol Infect . 2017;50(6):879-85.,2525. Stultz JS, Doern CD, Godbout E. Antibiotic resistance in pediatric urinary tract infections. Curr Infect Dis Rep. 2016;18(12):40.. These resistance rates may be explained by the frequent prescription of these antimicrobials in empirical treatment of UTIs.

UPEC strains have numerous virulence factors that enable bacteria to colonize the urinary tract and overcome various host defense mechanisms2626. Bien J, Sokolova O, Bozko P. Role of uropathogenic Escherichia coli virulence factors in development of urinary tract infection and kidney damage. Int J Nephrol. 2012;2012:681473.,2727. Ko¨ves B and Wullt B. The roles of the host and the pathogens in urinary tract Infections. Eur Urol Suppl. 2016;15(4):88-94.. In this study, 28.8% of the isolates were negative for examined genes. On the other hand, 71.2% of the isolates were positive for at least one of the virulence genes examined. Of these virulence factors, adhesion molecules have an important role in the promotion of colonization, invasion, and replication within uroepithelial cells2626. Bien J, Sokolova O, Bozko P. Role of uropathogenic Escherichia coli virulence factors in development of urinary tract infection and kidney damage. Int J Nephrol. 2012;2012:681473.. In this study, the most prevalent adhesion genes were papE-F (32.7%, n:50) and papC (26.1%, n: 40), followed by sfa (11.1%, n:17), afaE (1.3%, n:2), and afaD (1.3%, n:2), respectively. Presence of P fimbria is well documented to be associated with pyelonephritis and cystitis11. Paniagua-Contreras GL, Monroy-Perez E, Rodriguez-Moctezuma JR, Dominguez-Trejo P, Vaca-Paniagua F, Vaca S. Virulence factors, antibiotic resistancephenotypes and O-serogroups of Escherichia coli strains isolated from community acquired urinary tract infection patients in Mexico. J Microbiol Immunol Infect. 2015;50(4):478-85.. In a study conducted by Munkhdelger et al. (2017), the frequency of fimH, papC, papGII, afa/draBC, sfa/focDE and papGIII was 89.9%, 20.3%, 17.6%, 15.5%, 8.8% and 1.4% 2828. Munkhdelger Y, Gunregjav N, Dorjpurev A, Juniichiro N, Sarantuya J. Detection of virulence genes, phylogenetic group and antibiotic resistance of uropathogenic Escherichia coli in Mongolia. J Infect Dev Ctries. 2017;11(1):51-7.. In another study conducted in Brazil, Tiba et al. (2008) reported frequency of the virulence genes fimH, papC, sfa, and afa to be 97.5%, 32.7%, 27.8%, and 6.2%, respectively2929. Tiba MR, Yano T, Leite Dda S. Genotypic characterization of virulence factors in Escherichia coli strains from patients with cystitis. Rev Inst Med Trop Sao Paulo. 2008;50(5): 255-60.. In Mexico, Paniagua-Contreras et al. (2015) found the prevalence of fim, pap and papGII as 61.3%, 24.7%, and 21.1%, respectively11. Paniagua-Contreras GL, Monroy-Perez E, Rodriguez-Moctezuma JR, Dominguez-Trejo P, Vaca-Paniagua F, Vaca S. Virulence factors, antibiotic resistancephenotypes and O-serogroups of Escherichia coli strains isolated from community acquired urinary tract infection patients in Mexico. J Microbiol Immunol Infect. 2015;50(4):478-85.. The sfa gene was found in twelve (70.6 %) of the isolates together with pap genes. Shetty et al. (2014) explained that co-existence of these two genes are due to their localization on the same pathogenicity island of UPEC strains3030. Shetty AV, Kumar SH, Shekar M, Shetty AK, Karunasagar I, Karunasagar I. Prevalence of adhesive genes among uropathogenic Escherichia coli strains isolated from patients with urinary tract infection in Mangalore. Indian J Med Microbiol. 2014;32(2):175-8.. In addition, most of the isolates carried multiple adhesion genes, indicating that the isolates had the ability to adhere to the urinary tract and subsequently cause infection. It has been reported that ExPEC strains mainly belong to groups B2 and D, and have higher virulence genes in relation with isolates considered to be commensal, which belong to the phylogenetic groups A and B13131. Chapman TA, Wu X, Barchia I, Bettelheim KA, Driesen S, Trott D, et al. Comparison of virulence gene profiles of E. coli strains isolated from healthy and diarrheic swine. Appl Environ Microbiol . 2006;72(7):4782-95.,3232. 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(4):241-6.. Similarly, the phylogenetic groups D1 (29, 18.9%) and B23 (55, 35.9%) were the most common among the isolates carrying virulence genes in the study. In a study carried out in Mexico, Miranda-Estrada et al. (2017) reported that the majority of the isolates belonged to group B2 (60%) and harbored a high number of virulence factors3333. Miranda-Estrada LI, Ruíz-Rosas M, Molina-López J, Parra-Rojas I, González-Villalobos E, Castro-Alarcón N. Relationship between virulence factors, resistance to antibiotics and phylogenetic groups of uropathogenic Escherichia coli in two locations in Mexico. Enferm Infecc Microbiol Clin. 2017;35(7):426-33.. A similar result was reported in Pakistan by Bashir et al. (2012), who found 50% of UPEC isolates belong to group B2, and to a lesser extent, groups A1 and B1 (19%)3434. Bashir S, Haque A, Sarwar Y, Ali A, Anwar MI. Virulence profile of different phylogenetic groups of locally isolated community acquired uropathogenic E. coli from Faisalabad region of Pakistan. Ann Clin Microbiol Antimicrob. 2012;11:23.. Lee et al. (2015) also reported high prevalence of virulence factors in groups B2 (79.31%) and D (15.51%), followed by groups A (3.44%) and B1 (1.72%) in South Korea88. Lee JH, Subhadra B, Son YJ, Kim DH, Park HS, Kim JM, et al. Phylogenetic group distributions, virulence factors andantimicrobial resistance properties of uropathogenic Escherichia coli strains isolated from patients with urinary tract infections in South Korea. Lett Appl Microbiol. 2015;62(1):84-90.. On the other hand, in this study, 26.8% and 3.9% of the isolates were found to belong to the commensal groups A and D. Our results confirmed this hypothesis not only in ExPEC strains, but also in the commensal E. coli strains that can cause UTIs3535. Moreno E, Andreu A, Pérez T, Sabaté M, Johnson JR, Prats G. Relationship between Escherichia coli strains causing urinary tract infection in women and the dominant faecal flora of the same hosts. Epidemiol Infect. 2006;134(5):1015-23.,3636. 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.. In addition, Duriez et al. (2001) suggested that the distribution of B1, A and D groups in each population can vary according to various factors (geographic/climatic conditions, dietary factors, the use of antibiotics, host genetic factors) and commensal strains can acquire virulence factors and become potentially pathogenic3737. 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(Pt 6):1671-6..

In conclusion, various rates of resistance and virulence factors were determined among the isolates. Therefore, monitoring of E. coli isolates should be performed for the effective treatment of UTIs. The results of the study also revealed that E. coli isolates from UTIs belong to different phylogroups/subgroups (mainly B23), and harbor single or various virulence gene combinations. For this reason, more detailed studies are needed to determine the relationship between virulence traits and certain E. coli clones that cause UTIs in humans.

REFERENCES

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    Yun KW, Kim HK, Park HK, Kim W, Lim IS. Virulence factors of uropathogenic Escherichia coli of urinary tract infections and asymptomatic bacteriuria in children. J Microbiol Immunol Infect . 2014;47(6):455-61.
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    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.
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    Clermont O, Bonacorsi S, Bingen E. Rapid and simple determination of the Escherichia coli phylogenetic group. Appl Environ Microbiol. 2000;66(10):4555-8.
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    Giray B, Ucar F, Aydemir S. Genotypic analysis of Escherichia coli strains that cause urosepsis in the Aegean region. Turk J Med Sci . 2016;46(5):1518-27.
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    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.
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    Paykoc EI, Turkyilmaz S. Investigation of P fimbriae presence in Escherichia coli strains isolated from urine samples in human and their antibacterial resistance. Jundishapur J Microbiol. 2018;11(9):e66119.
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    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. Rev Soc Bras Med Trop. 2019;52:e20180499.
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    Procop G, Church D, Hall G, Janda W, Koneman E, Schrekenberger P, et al. Koneman’s color atlas and textbook of diagnostic microbiology.7th ed. Lippincott Williams and Wilkins: Philadelphia; 2017. 360-6 p.
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    Wang G, Clark CG, Rodgers FG. Detection in Escherichia coli of the genes encoding the major virulence factors, the genes defining the O157:H7 serotype, and components of the type 2 Shiga toxin family by multiplex PCR. J of Clinical Microbiology. 2002;40(10):3613-19.
  • 16
    Ahmed AM, Motoi Y, Sato M, Maruyama A, Watanabe H, Fukumoto Y, et al. Zoo animals as reservoirs of gram-negative bacteria harboring integrons and antimicrobial resistance genes. Appl Environ Microbiol . 2007;73(20):6686-90.
  • 17
    Yamamoto S, Tsukamoto T, Terai A, Kurazono H, Takeda Y, Yoshida O. Distrubiton of virulence factors in E. coli isolated from urine of cystitis patients. Microbiol Immunol. 1995; 39(6):401-4.
  • 18
    Bertin Y, Martin C, Oswald E, Girardeau JP. Rapid and specific detection of F17-related pili and adhesin genes in diarrheic and septicemic Escherichia coli strains by multiplex PCR. J Clin Microbiol. 1996;34(12):2921-8.
  • 19
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  • Limitation: This study’s limitation is the serogroup assay. Serogroup assays are used for accurate E. coli identification and for epidemiological investigations of E. coli outbreaks.
  • Ethical disclosure: Ethical approval was obtained from the Ethical Committee of Hatay Mustafa Kemal University (Protocol code: 2011/18-14). The authors declare that no experiments were performed on humans or animals for this study.
  • Financial Support: This study was granted by Hatay Mustafa Kemal University Scientific Research Fund (Project Number: 267).

Publication Dates

  • Publication in this collection
    07 Feb 2020
  • Date of issue
    2020

History

  • Received
    13 Sept 2019
  • Accepted
    17 Dec 2019
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