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 ~  Abstract
 ~ Introduction
 ~  Materials and Me...
 ~ Results
 ~ Discussion
 ~ Conclusions
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  Table of Contents  
Year : 2016  |  Volume : 34  |  Issue : 4  |  Page : 448-456

Distribution of virulence determinants among antimicrobial-resistant and antimicrobial-susceptible Escherichia coli implicated in urinary tract infections

Department of Basic Medical Sciences, Faculty of Medical Sciences, University of the West Indies, Kingston, Jamaica

Date of Submission30-May-2015
Date of Acceptance17-Jul-2016
Date of Web Publication8-Dec-2016

Correspondence Address:
P D Brown
Department of Basic Medical Sciences, Faculty of Medical Sciences, University of the West Indies, Kingston
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/0255-0857.195354

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 ~ Abstract 

Introduction: Uropathogenic Escherichia coli (UPEC) rely on the correlation of virulence expression with antimicrobial resistance to persist and cause severe urinary tract infections (UTIs).
Objectives: We assessed the virulence pattern and prevalence among UPEC strains susceptible and resistant to multiple antimicrobial classes.
Methods: A total of 174 non-duplicate UPEC strains from patients with clinically significant UTIs were analysed for susceptibility to aminoglycoside, antifolate, cephalosporin, nitrofuran and quinolone antibiotics for the production of extended-spectrum β-lactamases and for the presence of six virulence determinants encoding adhesins (afimbrial, Type 1 fimbriae, P and S-fimbriae) and toxins (cytotoxic necrotising factor and haemolysin). Results: Relatively high resistance rates to nalidixic acid, ciprofloxacin, cephalothin and trimethoprim-sulfamethoxazole (82%, 78%, 62% and 59%, respectively) were observed. Fourteen distinct patterns were identified for the virulence determinants such as afaBC, cnfI, fimH, hylA, papEF and sfaDE. The toxin gene, cnfI (75.3%), was the second most prevalent marker to the adhesin, fimH (97.1%). The significant association of sfaDE/hylA (P < 0.01) among antimicrobial resistant and susceptible strains was also observed notwithstanding an overall greater occurrence of virulence factors among the latter. Conclusions: This study provides a snapshot of UPEC complexity in Jamaica and highlights the significant clonal heterogeneity among strains. Such outcomes emphasise the need for evidence-based strategies in the effective management and control of UTIs.

Keywords: Adhesins, Escherichia coli, fluoroquinolone resistance, uropathogenic, virulence

How to cite this article:
Stephenson S, Brown P D. Distribution of virulence determinants among antimicrobial-resistant and antimicrobial-susceptible Escherichia coli implicated in urinary tract infections. Indian J Med Microbiol 2016;34:448-56

How to cite this URL:
Stephenson S, Brown P D. Distribution of virulence determinants among antimicrobial-resistant and antimicrobial-susceptible Escherichia coli implicated in urinary tract infections. Indian J Med Microbiol [serial online] 2016 [cited 2020 Apr 8];34:448-56. Available from:

 ~ Introduction Top

To date, urinary tract infections (UTIs) are among the most predominant nosocomial and community-acquired bacterial diseases in humans.[1],[2],[3] Cystitis and pyelonephritis are chronic uncomplicated forms of the disease and have been associated with a significant morbidity, high mortality and long-term sequelae subsequent to the impairment of renal function.[4] They are a common nuisance in females of all age groups, up to 50% of the women are reported to experience at least one UTI during their lifetime [4] and 16–25% of the women report recurrent UTIs within 6 months of an episode.[5] Annually, more than 1 million hospitalisations and US$1.6 billion are utilised for medical expenses.[6]

Occasionally, Escherichia coli, a commensal microbe of the intestinal tract, evolves to express a vast arsenal of virulence factors and strategies to promote its growth and persistence within the harsh environment presented by the host's urinary tract.[7] Patients harbouring anatomical defects of the urinary system due to abnormalities or medical treatment frequently fall victim to uropathogens that colonize the lower urinary zone.[2] Uropathogenic E. coli (UPEC) accounts for up to 90% of all UTIs [2] and are known to express multiple virulence determinants. Among these are various adhesins that mediate binding to specific uroepithelial cell and tissue receptors, and toxins utilised during dispersal via host organelles, or for nutrient accumulation and immune response cell incapacitation.[8],[9] Specifically, adhesins include Type 1, P- and/or S-pili, encoded by the respective fim, pap and sfa operons,[10] and toxins include the cytotoxic necrotising factor 1, haemolysin and secreted autotransporter toxin, encoded by cnf1, hylA and sat, respectively.[1],[11] UPEC strains thrive on host iron stores via the release of siderophores, aerobactin (aer) and iron-chelating factor (iroN).[2]

More recently, the dynamics involving pathogenicity and antimicrobial resistance has become an increasing global concern as the combination can significantly reduce drug treatment options and favourable outcomes. Multidrug resistance to several generations of aminoglycosides, cephalosporins, antifolates and fluoroquinolones, as well as the production of extended-spectrum β-lactamases (ESBLs) has been reported.[12] Fluoroquinolones, an empirical treatment alternative to trimethoprim-sulfamethoxazole (SXT) for nosocomial and community-acquired uncomplicated UTIs, have seen the emergence of resistance among uropathogens due to misuse.[2],[13] Mediated mainly by point chromosomal mutations in the quinolone resistance determining regions of DNA gyrase and topoisomerase IV and/or by plasmid-mediated mechanisms involving Qnr proteins, QepA efflux pumps or aminoglycoside acetyltransferase (aac[6']-lb-cr),[14] these mechanisms contribute significantly to quinolone resistance. Incidences of ciprofloxacin (CIP) resistance as high as 62%, 92% and 17.1% have been reported in Mexico, India and the USA, respectively.[2],[15],[16] On the other hand, resistance rates of up to 72.1% have been reported for SXT, a once widely used antifolate antibiotic for treating UTIs.[15]

In recent investigations, the association of pathogenicity with phenotypic or genotypic characterisation of fluoroquinolone resistance among UPEC has demonstrated a reduced virulence among resistant strains.[17] Such reports emphasise the dynamics of pathogenicity and warrant further investigation with respect to phylogenetic variation of strains from diverse geographic locations. To obtain a more comprehensive outlook on the potential risk posed by antimicrobial-resistant uropathogens, the connection of antimicrobial susceptibility, virulence pattern and distribution of the adhesins (afaBC, fimH, papEF and sfaDE) and toxins (cnfI and hylA) were investigated among UPEC strains that are resistant and susceptible to cephalothin (CF), cefotaxime (CTX), CIP, nalidixic acid (NAL), nitrofurantoin (F/M), tobramycin (NN) and SXT.

 ~ Materials and Methods Top

Bacterial strains

A total of 174 non-duplicate (one per patient) UPEC strains isolated from patients diagnosed with clinically significant UTI in Jamaica [18] were analysed in this study. Data collected for the study were limited in relation to the associated clinical features of the patient, but focused on phenotypic and genotypic characteristics of UPEC.

Antimicrobial susceptibility testing

Antimicrobial susceptibility testing was conducted by the standard disc diffusion technique according to the Clinical and Laboratory Standards Institute guidelines.[19] Strains susceptible or resistant to the aminoglycoside (10 µg NN), antifolate (1.25/23.75 µg SXT), cephalosporins (30 µg CF and 30 µg CTX), quinolones (30 µg NAL; 5 µg CIP) and the nitrofurans (300 µg F/M) were selected for further examination. ESBL production was investigated using ceftazidime/clavulanic acid and CTX/clavulanic acid discs (30/10 µg) alongside aztreonam discs (30 µg).

DNA isolation

Genomic DNA was recovered from bacterial strains subcultured overnight at 37°C on Luria Bertani (LB) agar with 40 µg/ml NAL by the boiling method.[8] Essentially, LB cultures were pelleted and cells were resuspended in 200 µl sterile distilled water prior to incubation at 100°C for 15 min. The resulting lysate was centrifuged to remove cellular debris, and the supernatant served as the template DNA stock.

Detection of virulence determinants

Polymerase chain reaction assays targeting virulence genes afaBC (afimbrial adhesion), cnfI (cytotoxic necrotic factor), fimH (Type 1 fimbriae), hylA (haemolysin), papEF (pyelonephritis-associated pili) and sfaDE (S-fimbriae) were carried out using the Promega GoTaq ® Green protocol (Promega, WI, USA) as indicated by the manufacturer using a GeneAmp 9700 Thermal Cycler (Applied Biosystems, USA). [Table 1] lists the primer sequences, amplicon sizes and annealing temperatures for the specific assays. Amplified products were detected by ultraviolet fluorescence following electrophoretic separation on ethidium bromide-stained 1.5% agarose gels, and sizes were estimated by comparison to positive controls and 1 kb (Bioneer Corporation, Republic of Korea) or 100 bp (Promega, WI, USA) molecular markers.
Table 1: Virulence determinants, primers and reaction characteristics used in this study

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Statistical analysis

Differences between virulence determinant distributions among strains were analysed using Chi-square and Fisher's exact tests. Pairwise analysis was conducted using SPSS software (version 20, SPSS Inc., USA). P < 0.05 was considered statistically significant in all cases.

 ~ Results Top

Antimicrobial susceptibility testing revealed 62.1%, 21.8%, 78.2%, 82.2%, 4.0% and 43.1% resistance rates to CF, CTX, CIP, NAL, F/M, NN and SXT, respectively [Table 2a], [Table 2b], [Table 2c]. Approximately, 31% of these strains were ESBL producers, and of these, almost 84% were multidrug-resistant to three or more classes of antibiotics. Most (95.4%) of the strains harboured at least one virulence gene [Table 3], and fimH was identified as the most common virulence gene (97.1%) [Figure 1]a, [Figure 1]b, [Figure 1]c and [Table 2]a, [Table 2]b, [Table 2]c. Frequencies of pap, afa and sfa were much lower: 12.6%, 10.4% and 9.2%, respectively. In addition, the presence of toxin genes cnfI and hylA was detected in 75.3% and 2.9%, respectively, of the strains. Eight strains did not harbour a virulence determinant.
Table 2a: Frequency of virulence determinants in quinolone-- and antifolate-susceptible and- -resistant Escherichia coli strains

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Table 2b: Frequency of virulence determinants in aminoglycoside -, cephalosporin- and nitrofurans-susceptible and-resistant Escherichia coli strains

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Table 2c: Presence of virulence determinant in extended-spectrum beta-lactamases-positive/negative and multidrug-susceptible and- -resistant E. coli strains

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Table 3: Number of virulence determinants harboured by uropathogenic Escherichia coli strains in this study

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Table 4: Virulence determinant patterns observed among antimicrobial-resistant and- -susceptible Escherichia coli strains in this study

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Figure 1: (a) Virulence determinant distribution among quinolone- and antifolate-resistant and -susceptible Escherichia coli strains in this study. (b) Virulence determinant distribution among cephalosporin-, aminoglycoside- and nitrofuran-resistant and -susceptible Escherichia coli strains in this study. (c) Virulence determinant distribution among extended-spectrum β-lactamase-positive/negative in addition to multidrug-resistant and -susceptible Escherichia coli strains in this study. *Significance where P < 0.05

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fimH, the most prevalent gene, demonstrated a similar frequency among the various classes of antimicrobial-resistant and antimicrobial-susceptible strains. Frequency of fimH presence among strains resistant to first- and second-generation quinolones and the antifolate ranged from 98.5% to 100% in NAL-R, CIP-R and SXT-R strains. For the respective susceptible strains, rates were slightly lower: 83.9–94.4% [Table 2]a. Similarly, frequencies of over 93.0% for CF-, CTX- and NN-resistant and NN-susceptible strains were observed [Table 2]b. Conversely, a lower rate (57.1%) was detected among the seven strains resistant to the nitrofuran. Further analysis revealed a significantly lower frequency of fimH among strains that were NN-R or NN-S (P < 0.05), or NAL- and F/M-susceptible and -resistant (P ≤ 0.001) when compared to CF-, CTX- CIP- and SXT-susceptible and -resistant strains [Table 2]. Conversely, there were higher rates of cnfI, papEF, afaBC, sfaDE and hylA in NAL-, CIP- and SXT-susceptible strains [Figure 1]a. Higher rates of the latter determinants were also detected in strains susceptible to NN (cnf1, papEF, sfaDE and hylA), cephalosporins (papEF, afaBC and hylA) and F/M (cnf1 and hylA) [Figure 1]b. In contrast, the occurrence of these virulence factors was more common among ESBL-producing strains (over 50% escalation for hylA, papEF and sfaDE) and marginally reduced among multidrug-resistant strains [Figure 1]c.

The general distribution of co-existing virulence genes in antibiotic-susceptible versus antibiotic-resistant strains illustrated in [Figure 2] highlights the predominance of fimH/cnfI among over 75% [Figure 2]a, 14–55% [Figure 2]b and 40–53% [Figure 2]c of drug-resistant strains. Other noteworthy combinations among resistant strains included fimH/papEF (0–11.9%), cnfI/papEF (4–8.4%), fimH/sfaDE (0.9–6.3%), fimH/afaBC (7.9–9.8%), cnfI/papEF (4–8.4%), cnfI/afaBC (7.9–9.9%), cnfI/sfaDE (0–6.3%), cnfI/fimH/papEF (4.0–8.4%), cnfI/fimH/sfaDE (0–7.0%) and afaBC/cnfI/fimH (5.9–9.8%). Similarly, fimH/cnfI was the most prevalent (73.5%) among the susceptible strains followed by fimH/papEF (1.5–21.1%), cnfI/papEF (10.2–22.2%), cnfI/afaBC (9.1–21.1%), afaBC/cnfI/fimH (8.3–21.1%) and cnfI/fimH/papEF (9.6–16.1%).
Figure 2: (a) Observed frequencies of co-occurrence of virulence determinants in nalidixic acid-, ciprofloxacin-, trimethoprim-sulfamethoxazole-resistant and -susceptible Escherichia coli strains. (b) Observed frequencies of co-occurrence of virulence determinants in cephalothin-, cefotaxime-, nitrofurantoin- and tobramycin-resistant and -susceptible Escherichia coli strains. (c) Observed frequencies of co-occurrence of virulence determinants in extended-spectrum β-lactamase positive/negative and multidrug-resistant and -susceptible Escherichia coli strains. *Significance where P < 0.05

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An analysis of the distribution of virulence determinants revealed 14 subtypes referred to as 'ST' [Table 4]. Characterised by the frequent coexistence of fimH and cnfI, ST3 was the most predominant pattern encountered (50.6%), followed by ST2 (18.4%). Within each putative pathotypic group, a significant statistical variation was identified more commonly for the co-occurrence of sfaDE/hylA (P < 0.01), papEF/hylA (P < 0.05), fimH/cnf1 (P < 0.05) and papEF/sfaDE (P < 0.05) [Figure 2]a, [Figure 2]b, [Figure 2]c. Specifically, the co-existence of sfaDE/hylA was more frequently associated with CF-, NAL-, CIP-, SXT- and multidrug-resistant strains (P < 0.05) in addition to CF-, CTX-, F/M-, NN-, SXT-susceptible and non-ESBL strains.{Table 6}

 ~ Discussion Top

UTIs are among the most prevalent diseases encountered worldwide.[22] The severity of infection is often dependent on the interplay between host susceptibility and virulence of the associated strain.[23] Hence, understanding the virulence properties of the pathogen aids in the evaluation of the potential outcome of infection and effective preventative measures. In light of these, virulence markers may serve as important epidemiological indicators in the detection and management of UTIs.[1],[3] Data from this study emphasise the complexity in virulence determinant distribution among UPEC in Jamaica.

Previous reports suggest a non-significant association of virulence with antimicrobial resistance in E. coli, particularly against the aminoglycosides and β-lactams, with the lower virulence prevalence being more associated with resistant strains.[24] This is despite the assumption that greater antimicrobial resistance should result in greater virulence.[2] However, albeit controversial, evidence points to an inverse relationship between quinolone and fluoroquinolone resistance and virulence factor distribution.[10] Hence, reduced virulence and pathogenicity among these resistant strains with the identification of a greater proportion of virulence genes in their susceptible counterparts have been demonstrated.[17],[22],[24],[25] This thesis may be in part based on the proposition that susceptible strains are fitter than their resistant counterparts due to reduced gyrase and topoisomerase efficiency.[13] Moreover, the formerly controversial attribution of virulence loss to quinolone resistance has now been largely accepted, based on the classic scenario surrounding the loss of β-haemolysis and P-fimbriae expression among NAL-resistant E. coli.[2],[17],[22],[25] Consequently, for this study, we focused on the analysis of frequency of virulence determinants among antifolate- and quinolone-susceptible and -resistant UPEC strains while examining significant trends or associations among other antimicrobial classes important in UTI therapy.

As previously reported, genes encoding fimbrial adhesion mechanisms are the most significant virulence factors in UPEC.[17],[23] Therefore, similar to other published data,[5],[17],[23]fimH was the most prevalent gene with significantly higher detection rates among susceptible strains, principally NN, CTX and F/M (P < 0.05). In contrast, there were significant decreases in occurrence among ESBL-producing, quinolone- and antifolate-susceptible versus -resistant strains, with statistically significant (P < 0.0001) lowered fimH expression among NAL-susceptible strains. It is speculated that a point mutation at codon 83 in the gyrA gene of quinolone- and fluoroquinolone-resistant strains influenced the consequential reduction in negative supercoiling, thus facilitating an increased expression of the fimH gene. This point mutation is thought to be conserved and disseminated in a clonal manner.[17] Alternately, it has been theorised that the frequency of virulence factors precedes resistance.[25] Hence, the increased occurrence of fimH among resistant strains may be a factor of phylogeny and intrinsic bacterial characteristics, the former of which was not investigated. Several phylogenetic studies have demonstrated the association of biotype B2 with UPEC strains resistant to the quinolones and fluoroquinolones.[25] However, the distribution of virulence factors among phylogenetic groups may vary according to geographical location, sample size and clinical source.[2]

With regard to afa, pap and sfa adhesins, as theorised, there were generally higher frequencies among NAL-, CIP- and SXT-susceptible strains. An opposing trend was observed among F/M-resistant strains harbouring afa, pap and sfa. In contrast to other data,[23],[26] there was an overall low detection of the P- and S-fimbriae genes in this study with the absence of a strong positive association between both adhesins, as reported elsewhere.[26] Comparable to one report,[12] the least common virulence determinants were afa, sfa, hyl and pap. Others reported that afa, pap and sfa frequencies include 6%, 25% and 26%, respectively, in Brazil [26] and 10–13%, 2–8% and 6–15%, respectively, in China.[27] Given that afimbrial adhesin (afa) and S-fimbriae (sfa) are usually associated with cystitis and pyelonephritis, while P-fimbriae are associated with pyelonephritis, we postulate that the vast majority of strains in this study were associated mainly with acute cystitis.[11],[23] Furthermore, these results suggest lowered probability of pathogenicity among these strains.[22]

Implicated in the modulation of signalling pathways, cell lysis, immune response dysfunction and cytoskeleton reorganisation,[28]cnf1 and hyl toxin genes (detected in 75% and 2.5% of all strains, respectively) were more associated with F/M-, NAL-, NN-, CIP- and SXT-susceptible strains. This contrasts with the reported detection rates of 37% and 81% for cnf1 and hyl, respectively.[14] Interestingly, like Type 1 fimbriae, cnf1, the second most prevalent determinant, also demonstrated higher frequencies among NAL-resistant, cephalosporin-resistant and ESBL-producing strains, though statistically insignificant. This phenomenon remains unclear and contributes to the complexity of virulence gene distribution and antibiotic resistance among UPEC strains.

Disparate to reports indicating up to 44% frequency among UPEC strains, the nearly absent hylA gene (2.9%) among resistant strains conflicts observations that suggest a physical association between cnfI and hylA on pathogenicity island (PAI) PIIJ96.[25],[29] The afa, cnf, hyl and sfa genes usually form clusters called PAIs harboured chromosomally or extrachromosomally.[2] Hence, the combination of two or more of these genes in strains may indicate possible linkage and the presence of a PAI. One example of such association was illustrated with sfaDE/hylA in CF-, CIP-, NAL- and SXT-resistant strains as well as CF-, CTX-, F/M-, NN- and SXT-susceptible strains (P < 0.01); this has been reported elsewhere for cnfI and sfa.[26] In addition, the finding of fimH/cnfI within over 73% of the UPEC strains in this study indicates a possible biased association and conservation of both determinants within this geographical location – a finding that has not been previously reported elsewhere.

The discrepancy in findings for cnf1 with other PAI-associated determinants (such as pap, afa, sfa and hyl) has been speculated to be a result of mutations conferring resistance, alongside chromosomal characteristics that cause eventual instability and loss of various regions within the associated PAI. Such variation in dissemination via genetic elements harbouring site-specific recombination systems may prove problematic in mapping pathotypes with antimicrobial resistance patterns.[30] Continuous exposure of UPEC strains to newer antibiotics such as fluoroquinolones facilitates the development of antimicrobial resistance, due to the excision or transposition of various regions of the chromosome.[17] This phenomenon may be influenced by the SOS pathway subsequent to quinolone activation, thereby contributing to the detection of fimH/cnf1, despite variation in virulence gene distribution.

Overall, of the 174 non-duplicate UPEC strains analysed, 95% carried at least one virulence determinant to produce 14 distinct patterns. With all six virulence genes identified, these results indicate a high heterogeneity with respect to virulence distribution among quinolone-, SXT-, cephalosporin-, aminoglycoside- and nitrofuran-susceptible and -resistant UPEC strains. The correlation between virulence gene presence and severity of UTIs has been established in some studies and may also serve as a useful tool in determining the pathophysiology of infection.[31] In addition, virulence factor frequency studies may assist in the development of novel non-antibiotic therapeutic strategies such as fimH or cnfI inhibitors. However, complexity brought about by variation due to intrinsic bacterial characteristics (such as chromosomal structure and level of stability against diverse environmental factors including antibiotic exposure, clinical conditions of the host and host susceptibility factors, as well as the pathogen's phylogenetic group) and geographical location cannot be excluded.

 ~ Conclusions Top

This is the first report on the association of virulence determinants with ESBL production, fluoroquinolone-, antifolate-, cephalosporin-, aminoglycoside- and nitrofuran-resistance among UPEC strains in Jamaica. Similar to other reports, we confirm the lower occurrence of virulence determinants among resistant strains except for the most prevalent determinant, fimH. With the identification of 14 virulence subtypes, this diversity serves as a reminder of the continued efforts required in properly monitoring uropathogens worldwide since the potential risk varies with geographical localisation. This study also emphasises the high frequency of resistance among this important uropathogen against first- and second-line antimicrobial agents used for the treatment of UTIs. These data should augment local, regional, and global awareness with regard to the health implications associated with a constant misuse of these drugs.


This work was supported by an intramural grant to SS from the Office of Graduate Studies and Research, University of the West Indies, Mona Campus, Jamaica.

Financial support and sponsorship

This work was supported by an intramural grant to SS from the Office of Graduate Studies and Research, University of the West Indies, Mona Campus, Jamaica.

Conflicts of interest

There are no conflicts of interest.

 ~ References Top

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  [Figure 1], [Figure 2]

  [Table 1], [Table 2a], [Table 2b], [Table 2c], [Table 3], [Table 4]


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2004 - Indian Journal of Medical Microbiology
Published by Wolters Kluwer - Medknow

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