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Prevalence of Plasmid-Mediated Quinolone Resistance (PMQRs) Determinants and Whole Genome Sequence Screening of PMQR-Producing E. coli Isolated from Men Undergoing a Transrectal Prostate Biopsy

Katarzyna Piekarska
Katarzyna Zacharczuk
Tomasz Wołkowicz
Rafał Gierczyński
Department of Bacteriology and Biocontamination Control, National Institute of Public Health NIH—National Research Institute, 24 Chocimska Str., 00-791 Warsaw, Poland
Author to whom correspondence should be addressed.
Int. J. Mol. Sci. 2022, 23(16), 8907;
Submission received: 30 June 2022 / Revised: 29 July 2022 / Accepted: 5 August 2022 / Published: 10 August 2022
(This article belongs to the Collection State-of-the-Art Molecular Microbiology in Poland)


Fluoroquinolones (FQs) are recommended as prophylaxis for men undergoing transrectal prostate biopsy (TRUS-Bx). Recent studies suggest a significant share of FQ-resistant rectal flora in post-TRUST-Bx infections. Methods: 435 Enterobacterales isolates from 621 patients attending 12 urological departments in Poland were screened by PCR for PMQR genes. PMQR-positive isolates were tested for quinolone susceptibility and investigated by whole genome sequencing (WGS) methods. Results: In total, 32 (7.35%) E. coli strains with ciprofloxacin MIC in the range 0.125–32 mg/L harbored at least one PMQR gene. qnrS and qnrB were the most frequent genes detected in 16 and 12 isolates, respectively. WGS was performed for 28 of 32 PMQR-producing strains. A variety of serotypes and sequence types (STs) of E. coli was noticed. All strains carried at least one virulence gene. AMR genes that encoded resistance against different classes of antibiotics were identified. Additionally, five of 13 ciprofloxacin-susceptible E. coli had alterations in codon 83 of the GyrA subunits. Conclusion: This study provides information on the common presence of PMQRs among E. coli, which may explain the cause for development of post-TRUS-Bx infections. High numbers of virulence and antimicrobial resistance genes detected show a potential for analysed strains to develop infections.

1. Introduction

Fluoroquinolones (FQs) are an important class of synthetic broad-spectrum antibacterial agents used in medicine for treatment of multiple infections. However, their increased use has led to increasing bacterial resistance, mainly among different species of Enterobacterales, creating a challenge for the effectiveness and safety of therapies used against infections caused by these bacteria.
Recently, the emerging threat of infectious complications after transrectal ultrasound-guided prostate biopsy (TRUS-Bx) has been reported [1,2,3]. The most common pathogen in the setting of post-biopsy infectious complications is Escherichia coli, with causative strains probably originating from the patient’s own endogenous flora [4]. Moreover, the prevention and management of TRUS-Bx infectious due to E. coli has become more complicated due to widespread emergence of FQ-resistant E. coli isolates. Such strains may be selected as a result of any FQ therapy or by FQ prophylaxis conventionally used prior to biopsy [5]. Studies suggest that pre-biopsy screening for such FQ-resistant pathogens, with subsequent “tailored” prophylaxis based on antimicrobial susceptibility results, may be an effective way to reduce infectious complications [1,6,7]. Therefore, there is a growing need to understand FQ-resistant strains by monitoring their prevalence and identifying predicting factors.
The main mechanism conferring high-level FQ resistance is the result of spontaneous point mutations within DNA gyrase and topoisomerase IV coding target enzymes for quinolones. A point mutation results in amino acid substitutions within the quinolone resistance determining region (QRDR) of gyrA and/or parC chromosomal genes encoding subunit A gyrase (GyrA) and subunit C (ParC) topoisomerase IV, respectively [8]. Although considerably less frequent, mutations in subunit B (GyrB) of DNA gyrase and subunit E (ParE) of topoisomerase IV have also been found to confer resistance to FQ. Meanwhile, in recent decades, plasmid-mediated quinolone resistance (PMQR) among Enterobacterales has become a global phenomenon [9]. PMQR mechanisms encoded by plasmid genes include Qnr peptides (capable of protecting DNA gyrase and topoisomerase IV from quinolones), aminoglycoside acetyl transferase aac(6′)-ib-cr (modifying quinolones with a piperazinyl substituent), and the quinolone efflux pumps—QepA and OqxAB [9]. The co-existence of mutations in QRDR and PMQR determinants in FQ-resistant Enterobacterales was described in previous works [9,10,11]. However, in the absence of chromosomally mediated quinolone resistance mechanisms (mutations), the acquisition of plasmid-mediated quinolone resistance mechanisms (PMQRs) leaves fluoroquinolones’ MIC values in the susceptible category, according to the EUCAST breakpoints criteria. It should also be noted that the presence of PMQRs has been found to promote QRDR mutations, increasing FQ resistance rates [9]. In addition, PMQRs transmitted on plasmids are capable of rapid spread between bacteria of different species, therefore giving rise to potential complications for the use of fluoroquinolones as therapy or prophylaxis. Consequently, the presence of PMQR-positive bacteria within rectums of patients undergoing biopsy are considered an important risk factor for complications and may pose a serious challenge to the treatment of infections.
Some studies have previously investigated the range of post-TRUS-Bx complications in the context of FQ resistance. Recently, our team published a study on the molecular mechanisms of FQ-resistance including the gyrA, gyrB and parC, parE mutations and PMQRs of Enterobacterales from rectal swabs of 48 men undergoing transrectal prostate biopsy [12]. Until recently, little has been known about the molecular properties of E. coli as causative agents of post-biopsy infections. Thus, we aimed to determine the prevalence of PMQR determinants in Enterobacterales strains isolated from rectal swabs of 621 men undergoing transrectal prostate biopsy at 12 urological hospitals in Poland. Then, we investigated PMQR-producing E. coli strains by WGS for antibiotic resistance genes, virulotype, and genotype, that potentially could be responsible for infections associated with post-TRUS-Bx complications in patients in Poland.

2. Results

2.1. Bacterial Isolates

A total of 435 Enterobacteriaceae strains were cultured from 621 rectal swabs of men undergoing prostate biopsy procedure, collected at 12 urological departments participating in the presented study. E. coli was the most prevalent gram-negative bacteria isolated. The main criterion for the selection of E. coli isolates for testing was the presence of PCR-product of the most commonly PMQRs i.e., qnrA, qnrB, qnrS, aac(6)-Ib-cr, and qepA.

2.2. Prevalence of Plasmid-Mediated Quinolone Resistance (PMQR) Determinants among Enterobacteriaceae Strains

A total of 435 Enterobacteriaceae strains were subjected to PCR screening for detecting PMQR genes. At least one PMQR determinant was present in 32 (7.35%) strains belonging solely to E. coli species (Table 1). The qnrS and qnrB were the most common PMQR determinants, detected in 17 (53.1%) and 12 (37.5%) of 32 E. coli isolates, respectively (Table 1). The aac(6)-Ib-cr gene was found in seven isolates (21.9%). Moreover, qnrB and aac(6)-Ib-cr, and qnrB and qnrS were detected in combination in two isolates each, respectively. In contrast, qnrA, qnrC, qnrD or qepA were not detected in any of the tested isolates.

2.3. Quinolone and Fluoroquinolone Susceptibility of Tested PMQR-Positive E. coli Isolates

E. coli susceptibility profiles for nalidixic acid and ciprofloxacin are summarised in Table 1. All 32 PMQR-positive clinical E. coli isolates were resistant to nalidixic acid. Additionally, 18 of the tested isolates were also resistant to ciprofloxacin. In isolates resistant to nalidixic acid only, the ciprofloxacin MIC range was 0.125–0.25 mg/L, in contrast to E. coli strains resistant to both nalidixic acid and ciprofloxacin where the ciprofloxacin MIC was ≥1.5 mg/L. Among 14 ciprofloxacin-susceptible E. coli isolates with ciprofloxacin MIC ranges (0.125 mg/L–0.25 mg/L), qnrB (n = 5) and qnrS (n = 11) were detected, and two isolates carried both determinants. However, in 18 ciprofloxacin-resistant E. coli with ciprofloxacin MIC ≥ 1.5 mg/L, three different PMQR determinants were detected including qnrB (n = 6), qnrS (n = 7), and aac(6)-Ib-cr (n = 7) (Table 1). Two E. coli isolates with ciprofloxacin MIC ≥24 mg/L carried a combination of qnrB and aac(6)-Ib-cr.

2.4. Whole Genome Sequencing Analysis of PMQR-Positive E. coli Strains

Data of whole genome sequencing analysis of 28 PMQR-positive E. coli isolated from rectal swabs of men undergoing transrectal prostate biopsy are presented in Table 2. Notably, nearly all genomes (except one) sequenced using the Nanopore platform were assemble into one large circular chromosome with few plasmids, which were usually also circular. For these strains, the chromosome size ranged from 4,544,229 bp to 5,258,810 bp (with an average of 4,895,805 bp). All these strains had 1–13 plasmids (with an average of five plasmids) and on average one of them was large (>100 kb). Among all 28 PMQR-positive E. coli tested, seven (IncFI, IncFII, IncX, IncI, IncY, IncN, Col types) plasmid replicons were identified with different frequencies (Table 2).
Hypothetical pathogenic potential of analysed strains were confirmed by the PathogenFinder tool, with minimal and maximal probability of being a human pathogen estimated at 0.919 and 0.943 respectively (with an average of 0.93).
All genomes were deposited in the GenBank database under BioProject no PRJNA861130.
Genotypic analysis of fluoroquinolone resistance. Point mutations involving amino acid substitutions among PMQR-positive E. coli were detected in 21 isolates out of 28 sequenced (Table 2). The substitutions were observed in two codons of GyrA: 83 (Ser → Leu) and 87 (Asp → Asn); in three codons of ParC: 56 (Ala → Thr), 80 (Ser → Ile), and 84 (Glu→Gly, Val); in three codons of ParE: 416 (Leu → Phe), 458 (Ser → Ala) and 529 (Ile→Leu), respectively. No substitution was observed in the GyrB subunit in any of the isolates tested. The Ser83 → Leu mutation in the GyrA was the most common in PMQR-positive E. coli isolates, and was found in 20 isolates with a ciprofloxacin MIC at 0.125 → 32 mg/L, including five isolates of 13 susceptible to ciprofloxacin with ciprofloxacin MIC < 0.5 mg/L. The second most widespread gyrA mutation was Asp87 → Asn, found among 11 isolates. In parC, the most frequent mutation was Ser80→Ile, found in 12 isolates. Other identified mutations were observed infrequently. The PMQR-positive E. coli isolates resistant to ciprofloxacin with MIC > 4 mg/L had two or more substitutions, found in GyrA, ParC, and ParE (Table 2). Among genes encoding plasmid-mediated FQ resistance, qnrS1, qnrB19, and aac(6′)-Ib-cr were identified in 12, two, and three tested isolates, respectively.
Analysis of genes predicted to confer resistance to other antibiotics. According to the WGS analysis shown, 37 different determinants of resistance were identified (Table 2). Among genes encoding β-lactam resistance were detected blaTEM-1B in 14 isolates, blaOXA-1 in three isolates, blaTEM-CTX-M-15 in two isolates, and blaTEM-1C, blaTEM-1D, blaTEM-84, blaTEM-30, blaTEM-32, blaTEM-135 in one isolate each. Seven genes encoding resistance to aminoglycosides were detected, including aph(3′′)-Ib (n = 7 isolates), aph(6)-Id (n = 7 isolates), aadA1 (n = 5 isolates), aadA5 (n= 4 isolates), ant(3′′)-Ia (n = 2 isolates), aph(3′)-Ia (n = 1 isolate) and ant(3′′)-Ia (n = 1 isolate). Genes encoding sulphonamides resistance totalled nine for sul1, eight for sul2 and one for sul3 and trimethoprim, five for drfA1, two for drfA17, and one each for drfA7 and drfA15. Three genes encoding resistance to macrolides, namely mdfA, mphA, and mphB were identified in 11, three and one isolate, respectively. Tetracycline resistance encoded by tetA and tetB genes was identified in 11 and 5 isolates, respectively. Genes encoding chloramphenicol resistance numbered three for catB3, two for cmlA1, and one each for catA1 and floR. Moreover, in 17 of the E. coli isolates tested, an operon sitABCD encoding a member of the family of ATP-binding cassette divalent metal ion transporters was identified.
Virulence genes analysis. At least one virulence gene was detected among all sequenced E. coli isolates (Table 2). Table 3 summarises the distribution of 53 different virulence genes identified in 28 PMQR-positive E. coli samples, both sensitive and resistant to ciprofloxacin. No significant differences were found in the occurrence of virulence factors among the resistant and susceptible strains of E. coli tested. All tested E. coli isolates possessed gad (glutamate decarboxylase). The other most frequent virulence genes, identified among ≥10 E. coli sequenced isolates, were terC (tellurium ion resistance protein), iss (increased serum survival), sitA (iron transport protein), ompT (outer membrane protease-protein protease 7), traT (outer membrane protein complement resistance), fyuA (siderophore receptor), irp2 (high molecular weight protein 2 non-ribosomal peptide synthetase), iucC (aerobactin synthetase), iutA (ferric aerobactin receptor), iroN (enterobactin siderophore receptor protein), and hlyF (hemolysin F) (Table 3).
MLST and serotyping. Out of the total of 28 E. coli isolates, 19 different STs were identified (Table 2). E. coli most often belonged to ST131, observed in four out of 28 tested isolates, and each of ST88, ST162, ST428, ST10, and ST46 was observed in two E. coli isolates. Four E. coli belonged to ST131, of serotypes O25:H4 (n = 3) and O16:H5 (n = 1), respectively. E. coli in ST88, ST428, ST10, and ST46 had the serotypes O8:H17, O117:H4, O101:H9, and O9:H10, respectively. ST162 in two E. coli had a different serotype i.e., O9:H19 and O33:H25. Each of ST69, ST38, ST82331, ST2207, ST1125, ST683, ST2064, ST206, ST224, ST117, ST90, ST95, and ST617 was observed in one of the 28 E. coli tested, respectively.

3. Discussion

The genetic profiling of clinical strains can provide useful information about their potential for causing disease and resistance to treatment. This study investigated the prevalence of PMQR determinants and the WGS of PMQR-positive Enterobacterales strains isolated from men undergoing prostate biopsy procedures, collected at 12 urological departments in Poland. These isolates exhibited a diverse range of serotypes, sequence types (ST), virulotypes, and antimicrobial-resistant gene profiles.
In general, current data shows the prevalence of PMQR determinants in 7.35% of Enterobacterales isolates, with some qnrB and qnrS genes found in E. coli isolates susceptible to FQs (ciprofloxacin MICs 0.125–0.25 mg/L). These findings correspond with the popular hypothesis that PMQR determinants may promote mutations in the quinolone resistance-determining region (QRDR) and, consequently, increase quinolone resistance in clinical settings, so that their presence may significantly contribute to the occurrence of post-biopsy complications [8,9,10]. Moreover, the findings strongly confirm the need to perform microbiological diagnostic tests (including PCR on PMQRs) before a biopsy, which has also been suggested by other authors [13,14,15].
According to the European Association of Urology (EAU), it is highly recommended to use antimicrobial prophylaxis in men prior to a transrectal prostate biopsy (TRUS-Bx), to minimise the risk of bacterial infection after the procedure [5]. All patients in our study from whom PMQR-producing isolates were collected received ciprofloxacin orally 2 h prior to the procedure. It should be noted that the PMQR resistance traits found in FQ-susceptible E. coli strains from patients receiving ciprofloxacin prophylaxis prior to TRUS-Bx indicated that FQ prophylaxis or treatment of post-biopsy complications may be ineffective in patients who carry PMQR-positive strains, and in consequence may promote development of high-level FQ resistance.
In our data, qnrS1 was dominant (78.6%) among ciprofloxacin-susceptible E. coli isolates, while qnrB was detected in 35.7% of such isolates. In the ciprofloxacin-resistant E. coli group with ciprofloxacin MIC ≥ 1.5 mg/L, qnrB and aac(6)-Ib-cr determinants were dominant and were the same types of PMQRs reported for FQ resistant strains in other reports, [10,16]. These differences in proportions of different qnrs may provide additional premises for two probable means of selection of PMQR-positive strains playing essential roles in acquisition of quinolone resistance—foodborne and environmental (qnrS), or medical care (qnrB, aac(6)-Ib-cr). Studies have suggested that the agricultural use of antimicrobial agents increased the number of human infections caused by drug-resistant bacteria [17]. Furthermore, consumption of food contaminated by PMQR-positive strains or use of FQs in ambulatory and hospital therapy may promote pre-selection factors for FQ resistance [12].
In many studies of the causes of post-biopsy complications, collections of FQ-resistant isolates have been investigated [1,2,3,18]. In those studies, FQ-resistant E. coli were found to occur frequently in strains isolated from men undergoing TRUS-Bx. In this prospective study, the only selection criterion was prevalence of PMQR. However, we found that 82 (18.8%) of the investigated E. coli strains were resistant to ciprofloxacin, with MIC > 0.5 mg/L. Differences in ciprofloxacin-resistance rates between patients from 12 urological centres were observed. The ciprofloxacin MICs for the 82 selected ciprofloxacin-resistant E. coli were in the range 0.75–>32 mg/L. The vast majority (n = 44; 53.7%) of ciprofloxacin-resistant isolates had ciprofloxacin MIC > 32 mg/L (data not shown).
WGS showed a huge variation among E. coli strains tested, as assessed by multi-locus sequence typing (MLST) and serotyping. In the present study, E. coli strains O25:H4 ST131 were found to predominate among other 19 STs detected, as shown in Table 2. One strain ST131 had a different serotype within it i.e., O16:H5. However, ST131 E. coli isolates of serotype O16:H5 have also been identified in Japan, Denmark, Australia, and France [19,20,21,22]. Nowadays, ST 131 has been identified as the predominant E. coli lineage among extraintestinal pathogenic E. coli (ExPEC) isolates worldwide. E. coli ST131 isolates have been reported to produce extended-spectrum β-lactamases (ESBL), such as CTX-M-15 or non-ESBL-produce; almost all are resistant to fluoroquinolones and ampicillin/amoxicillin, and are often resistant to aminoglycosides, macrolides, chloramphenicol and tetracyclines [23]. In our study, three isolates of E. coli ST131 serotype O25:H4 showed high-level resistance to ciprofloxacin (MIC > 32 mg/L) and had at least four amino acid substitutions in GyrA and ParC. Additionally, those isolates contained the aac(6)-Ib-cr PMQR gene, CTX-M-15 (ESBL), OXA-1 conferring to resistance to ampicillin/amoxicillin, and mphA conferring resistance to macrolide. Isolate no. F078 E. coli ST131 O16:H5 was susceptible to ciprofloxacin (MIC 0.25 mg/L), but had substitutions in GyrA and ParE and possessed genes conferring to resistance to aminoglycosides (aadA, aph(6)-Id, aph(3′′)-Ib), trimethoprim (drfA), sulphonamides (sul1, sul2), tetracyclines (tetA), macrolides (mphA, mdfA), and qnrS detected by PCR. It should be highlighted that the multidrug-resistant ST131 clonal group was found to account for 70% of FQ-resistant rectal E. coli isolates among men undergoing transrectal prostate biopsy in the USA [24].
Other STs frequently detected in our study were ST88 (serotype O8:H17), ST162, ST428 (serotype O117:H4), ST10 (serotype O101:H9) and ST46 (serotype O9:H10). Each was found in two isolates, although ST162 had different serotypes i.e., O9:H19 and O33:H25. It should be noted that, in addition toST131, ST69, ST38, ST88, ST117, ST10, ST95, and ST617 are also major STs globally noted among ExPEC isolates [25].
In general, the potential of antimicrobial resistance in E. coli isolates tested was found to be significant. Based on the identified resistance genes, the majority of tested isolates contained at least one determinant conferring resistance. The most frequently identified genes were blaTEM, conferring resistance to β-lactams. Resistance to ampicillin/amoxicillin in E. coli isolates is widespread and may be mediated by production of plasmid-encoded TEM-1/2, SHV-1, or OXA-1 enzymes [23]. In our study, 16 of 28 E. coli isolates possessed the blaTEM-1 gene. Additionally, in four isolates we identified other blaTEM genes encoding β-lactamase i.e., blaTEM-84, blaTEM-30, blaTEM-32, blaTEM-135. Moreover, as shown in Table 2, genes conferring resistance to aminoglycosides (aph(3′′)-Ib, aph(6)-Id, aad), tetracyclines (tetA, tetB), macrolides (mdf, mph), sulphonamides (sul), and trimethoprim (drf) were common in the tested strains.
E. coli is a heterogeneous species that encompasses strains with various degrees of pathogenicity as well as non-pathogenic strains. The performed analysis confirmed that all the analyzed strains had theoretical pathogenic potential. Pathogenic E. coli are divided into two major groups, associated with intestinal and extra-intestinal diseases [26,27]. The extra-intestinal E. coli pathotypes cause urinary tract infections, neonatal meningitidis and septicemia [26]. The current study also characterised virulence genes in all PMQR-positive E. coli isolates from men undergoing prostate biopsy. Among 53 different virulence genes identified in all tested E. coli isolates, the highest frequencies were gad, terC, iss, sitA, ompT, traT, fyuA, irp2, iucC, iutA, iroN, and hlyF, some of which have been reported in pathogenic E. coli isolates [28]. However, the presence of single or multiple virulence genes does not confirm that a strain is pathogenic, unless that strain has the appropriate combination of virulence genes to cause infection in a host [29]. To cause infection, pathogenic E. coli isolates use a complex multistep mechanism of pathogenesis involving a number of virulence factors which consist of attachment, host cell surface modification, invasion, a variety of toxins, and secretion systems [30]. Thus, virulence factors are ideal target for determining the pathogenic potential of a given E. coli isolate [31]. Based on this finding, routine screening of bacteria isolated from men undergoing prostate biopsy can improve clinical significance.
It is worth noting that in this study, among 17 E. coli isolates tested, an operon sitABCD was identified encoding a member of the family of ATP-binding cassette divalent metal ion transporters. The operon sitABCD is homologous to avian pathogenic E. coli isolate, and mediates transport of iron and manganese as well as resistance to hydrogen peroxide. Starowska et al. [32] indicated the possibility of replacement of virulence genes located on mobile genetic elements between human and avian pathogenic E. coli strains, and that with them could be transferred genes encoding resistance to antimicrobials, ions, and other chemical components.
A limitation of our research was the performance of WGS analysis four years after susceptibility testing and PCR. This could have significantly influenced on the observed lack of correlation between the PMQR genes detected by the PCR method and the WGS analysis. qnr genes are localized on mobile elements and their presence can be affected by over-stabilizing the DNA-helicase complexes. Thus, they could be lost during laboratory manipulations without antimicrobial pressure. Such a situation has also been noticed by other scientists (personal communication during ECDC/EFSA fourth joint meeting on AMR for the FWD-Network and EURL-AR Network). This remains a hypothesis, and its verification needs further investigation.
In conclusion, by using whole genome sequencing, we obtained valuable information about bacterial strains and demonstrated that WGS can be a valuable early warning system for emerging resistance mechanisms and potential therapeutic failure. Our data also suggest that antimicrobial resistance is a potentially more important trait than virulence in terms of increased risk of post-biopsy infection. This is in line with the findings of other authors [33]. Meanwhile, the molecular characteristics including virulence and presence of antimicrobial resistance genes show the considerable potential of the investigated E. coli in the development of infection.

4. Materials and Methods

4.1. Bacterial Strains, Antimicrobial Susceptibility Testing and PCR

A prospective study was conducted between April and December 2016 at 12 urological departments in Poland. Ethics approval was obtained from the local ethics committee of the National Institute of Public Health National Institute of Hygiene (Research Ethics Committee No. 4/2015 from 2 December 2015), Warsaw, Poland. Rectal swabs were collected from 621 patients undergoing transrectal prostate biopsy. The samples were suspended in BHI broth with 20% glycerol, frozen at −20 °C and transported frozen to our laboratory. Rectal swabs were streaked onto a MacConkey agar plate (Oxoid Ltd., Basingstoke, UK) and were incubated at 37 °C for 24 h in aerobic conditions. From each plate with gram-negative bacterial growth, a representative colony of each distinct morphotype was selected for species identification by classical biochemical tests. Screening for qnrA, qnrB, qnrS, aac(6)-Ib-cr, and qepA genes as more common PMQRs was carried out for all selected strains by using PCR as described previously [10].
All PMQR-positive isolates were screened with ciprofloxacin (5 μg) and nalidixic acid (30 μg) (Oxoid Ltd., Basingstoke, UK) on Mueller-Hinton agar (Oxoid Ltd., Basingstoke, UK). In addition, the E-test (bioMerieux, Marcy l‘Etoile, France) method was used in all PMQR-positive isolates to determine the minimum inhibitory concentration (MIC) of ciprofloxacin. The susceptibility results were interpreted according to European Committee on Antimicrobial Susceptibility (EUCAST) criteria (, accessed on 1 January 2022), and a zone of inhibition around the ciprofloxacin disc (<22 mm) along with MIC of ciprofloxacin >0.5 mg/L were classified as resistance to FQs. The MIC for each isolate was measured at least twice.

4.2. Whole Genomes Sequencing (WGS)

Twenty-eight of the PMQR-positive isolates recovered in this study were subjected to whole genome sequencing analysis (WGS). All steps of the WGS (DNA purification, library preparation and sequencing) were performed at the National Institute of Public Health NIH—National Research Institute. Libraries for 13 strains were prepared using an Illumina DNA Prep Kit (Illumina Inc., San Diego, CA, USA). The libraries were sequenced on an Illumina MiSeq sequencer (Illumina Inc.) using 150-bp paired-end reads. Libraries for another 15 strains were prepared using a Nanopore Rapid Barcoding Kit, and the whole genome sequencing was performed on GridION (Oxford Nanopore Technologies, Oxford, UK). Genomes were assembled using CLC Genomics Workbench 22 (for strains sequenced on Illumina) and the NanoForms server (for strains sequenced on Nanopore [34]). Species confirmation, multilocus sequence typing (MLST), serotyping, virulence and AMR (Antimicrobial Resistance) genes, and plasmid replicons were analysed using SpeciesFinder 2.0 [35], MLST 2.0 [36], SerotyperFinder 2.0 [37], VirulenceFinder 2.0 [38], ResFinder 4.1 [39], respectively, available on the Centre for Genomic Epidemiology website (, accessed on 1 January 2022). Additionally, the hypothetical pathogenic potential was estimated by proteome analysis using PathogenFinder 1.1 [40].

Author Contributions

K.P. was responsible for the design of this study and choice of methods, data analysis, check and manuscript draft. K.Z. was responsible for phenotypic analysis, including strains isolation and identification, antibiotic susceptibility testing and PCR experiments and data analysis, performed WGS experiments. T.W. was responsible for performed WGS experiments, data analysis and participation in writing of the WGS part of the manuscript. R.G. was the main reviewer and editor of the final version of the manuscript. All authors have read and agreed to the published version of the manuscript.


This research was partially supported by internal-grant from the National Institute of Public Health—National Institute of Hygiene (no. 4/EM/2017).

Institutional Review Board Statement

The study was conducted in accordance with the Declaration of Helsinki, and approved by Ethics Committee of the National Institute of Public Health-National Institute of Hygiene, Warsaw, Poland (protocol code No. 4/2015 of 2 December 2015).

Informed Consent Statement

Informed consent was obtained from all subjects involved in the study.

Data Availability Statement

All data are presented within the article. The authors confirmed that personal identity information of the patients was unidentifiable from this report.


The authors would like to thank Mateusz Mokrzyś and Stanisław Szempliński, for help in organizing the study at 12 urology clinics and for the collection of research material; Magdalena Nowakowska and Natalia Wolaniuk, M.Sc. for technical assistance in performing PCR, identification and antimicrobial susceptibility testing of microorganisms isolated.

Conflicts of Interest

The authors declare no conflict of interest.


  1. Williamson, D.A.; Barrett, L.K.; Rogers, B.A.; Freeman, J.T.; Hadway, P.; Paterson, D.L. Infectious complications following transrectal ultrasound-guided prostate biopsy: New challenges in the era of multidrug-resistant Escherichia Coli. Clin. Infect. Dis. 2013, 57, 267–274. [Google Scholar] [CrossRef] [Green Version]
  2. Sieczkowski, M.; Gibas, A.; Bronk, M.; Matuszewski, M. Fluoroquinolone-based antimicrobial prophylaxis in patients undergoing transrectal ultrasound-guided prostate biopsy. Eur. J. Clin. Microbiol. Infect. Dis. 2015, 34, 1815–1821. [Google Scholar] [CrossRef] [Green Version]
  3. Suwantarat, N.; Rudin, S.D.; Marshall, S.H.; Hujer, A.M.; Perez, F.; Hujer, K.M.; Domitrovic, T.N.; Dumford, D.M., 3rd; Donskey, C.J.; Bonomo, R.A. Infections caused by fluoroquinolone-resistant Escherichia coli following transrectal ultrasound-guided biopsy of the prostate. J. Glob. Antimicrob. Resist. 2014, 2, 71–76. [Google Scholar] [CrossRef] [Green Version]
  4. Cussans, A.; Somani, B.K.; Basarab, A.; Dudderidge, T.J. The role of targeted prophylactic antimicrobial therapy before transrectal ultrasonography-guided prostate biopsy in reducing infection rates: A systematic review. BJU Int. 2016, 117, 725–731. [Google Scholar] [CrossRef] [Green Version]
  5. Bonkat, G.; Bartoletti, R.; Bruyère, F.; Cai, T.; Geerlings, S.E.; Köves, B.; Schubert, S.; Wagenlehner, F. European Association of Urology (EAU) on Urological Infections Guidelines; Edn. Presented at the EAU Annual Congress Amsterdam the Netherlands 2020; EAU Guidelines Office: Arnhem, The Netherlands, 2020; ISBN 978-94-92671-07-3. Available online: (accessed on 20 March 2020).
  6. Hadjipavlou, M.; Eragat, M.; Kenny, C.; Pantelidou, M.; Mulhem, W.; Wood, C.; Dall’Antonia, M.; Hammadeh, M.Y. Effect of augmented antimicrobial prophylaxis and rectal swab culture-guided targeted prophylaxis on the risk of sepsis following transrectal prostate biopsy. Eur. Urol. Focus. 2015, 6, 95–101. [Google Scholar] [CrossRef]
  7. Taylor, A.K.; Zembower, T.R.; Nadler, R.B.; Scheetz, M.H.; Cashy, J.P.; Bowen, D.; Murphy, A.B.; Dielubanza, E.; Schaeffer, A.J. Targeted antimicrobial prophylaxis using rectal swab cultures in men undergoing transrectal ultrasound guided prostate biopsy is associated with reduced incidence of postoperative infectious complications and cost of care. J. Urol. 2012, 187, 1275–1279. [Google Scholar] [CrossRef]
  8. Hopkins, K.; Davies, R.H.; Threlfall, E.J. Mechanisms of quinolone resistance in Escherichia coli and Salmonella: Recent developments. Int. J. Antimicrob. Agents. 2005, 25, 358–373. [Google Scholar] [CrossRef]
  9. Rodríguez-Martínez, J.M.; Machuca, J.; Cano, M.E.; Calvo, J.; Martínez-Martínez, L.; Pascual, A. Plasmid-mediated quinolone resistance: Two decades on. Drug Resist. Updat. 2016, 29, 13–29. [Google Scholar] [CrossRef]
  10. Piekarska, K.; Wołkowicz, T.; Zacharczuk, K.; Rzeczkowska, M.; Chróst, A.; Bareja, E.; Olak, M.; Gierczyński, R. Co-existence of plasmid-mediated quinolone resistance determinants and mutations in gyrA and parC among fluoroquinolone-resistant clinical Enterobacteriaceae isolated in a tertiary hospital in Warsaw, Poland. Int. J. Antimicrob. Agents. 2015, 45, 238–243. [Google Scholar] [CrossRef]
  11. Vinué, L.; Hooper, D.C.; Jacoby, G.A. Chromosomal mutations that accompany qnr in clinical isolates of Escherichia coli. Int. J. Antimicrob. Agents. 2018, 51, 479–483. [Google Scholar] [CrossRef]
  12. Piekarska, K.; Zacharczuk, K.; Wołkowicz, T.; Mokrzyś, M.; Wolaniuk, N.; Nowakowska, M.; Szempliński, S.; Dobruch, J.; Gierczyński, R. Molecular mechanisms of fluoroquinolones resistance found in rectal swab isolates of Enterobacterales from men undergoing transrectal prostate biopsy: A rationale for directed prophylaxis. Ann. Clin. Microbiol. Antimicrob. 2021, 20, 81. [Google Scholar] [CrossRef]
  13. Roberts, M.J.; Williamson, D.A.; Hadway, P.; Doi, S.A.R.; Gardiner, R.A.; Peterson, D.L. Baseline prevalence of antimicrobial resistance and subsequent infection following prostate biopsy using empirical or altered prophylaxis: A bias-adjusted meta-analysis. Int. J. Antimicrob. Agents. 2014, 43, 301–309. [Google Scholar] [CrossRef]
  14. Johansen, T.E.B.; Zahl, P.H.; Baco, E.; Bartoletti, R.; Bonkat, G.; Bruyere, F.; Cai, T.; Cek, M.; Kulchavenya, E.; Köves, B.; et al. Antibiotic resistance, hospitalizations, and mortality related to prostate biopsy: First report from the Norwegian patient registry. World J. Urol. 2020, 38, 17–26. [Google Scholar] [CrossRef] [PubMed]
  15. Lee, K.; Drekonja, D.M.; Enns, E.A. Cost-effectiveness of antibiotic prophylaxis strategies for transrectal prostate biopsy in an era of increasing antimicrobial resistance. Value Health. 2018, 21, 310–317. [Google Scholar] [CrossRef] [Green Version]
  16. Kotb, D.; Khairby, W.; Mahmud, M.S.; Khairy, R.M.M. Impact of co-existence of PMQR genes and QRDR mutations on fluoroquinolones resistance in Enterobacteriaceae strains isolated from community and hospital acquired UTIs. BMC Infect. Dis. 2019, 19, 979. [Google Scholar] [CrossRef]
  17. O’Neel, J. Antimicrobials in agriculture and the environment: Reducing unnecessary use and waste. Review on antimicrobial resistance. 2015. Available online: (accessed on 8 December 2015).
  18. Adamczyk, P.; Juszczak, K.; Prondzinska, M.; Kędzierska, A.; Szwajkert-Sobiecka, H.; Drewa, T. Fluoroquinolone-resistant Escherichia coli in intestinal flora of patients undergoing transrectal ultrasound-guided prostate biopsy—possible shift in biopsy prophylaxis. Cent. Eur. J. Urol. 2017, 70, 192–196. [Google Scholar]
  19. Matsumura, Y.; Yamamoto, M.; Nagao, M.; Hotta, G.; Matsushima, A.; Ito, Y.; Takakura, S.; Ichiyama, S. Emergence and spread of B2-ST131-O25b, B2-ST131-O16 and D-ST405 clonal groups among extended-spectrum β-lactamase-producing Escherichia coli in Japan. J. Antimicrob. Chemother. 2012, 67, 2612–2620. [Google Scholar] [CrossRef] [Green Version]
  20. Olesen, B.; Hansen, D.S.; Nilsson, F.; Frimodt-Moller, J.; Leihof, R.F.; Struve, C.; Scheutz, F.; Johnston, B.; Krogfelt, K.A.; Johnson, J.R. Prevalence and characteristics of the epidemic multiresistant Escherichia coli ST131 clonal group among extended-spectrum β-lactamase-producing E. coli isolates in Copenhagen, Denmark. J. Clin. Microbiol. 2013, 51, 1779–1785. [Google Scholar] [CrossRef] [Green Version]
  21. Blanc, V.; Leflon-Guibout, V.; Blanco, J.; Haenni, M.; Madec, J.-Y.; Rafignon, G.; Bruno, P.; Mora, A.; Lopez, C.; Dahbi, G.; et al. Prevalence of day-care centre children (France) with faecal CTX-M-producing Escherichia coli comprising O25b:H4 and O16:H5 ST131 strains. J. Antimicrob. Chemother. 2014, 69, 1231–1237. [Google Scholar] [CrossRef]
  22. Kudinha, T.; Johnson, J.R.; Andrew, S.; Kong, F.; Anderson, P.; Gilbert, G.L. Escherichia coli sequence type 131 (ST131) as a prominent cause of antibiotic resistance among urinary Escherichia coli isolates from reproductive-age women. J. Clin. Microbiol. 2013, 51, 3270–3276. [Google Scholar] [CrossRef] [Green Version]
  23. Nicolas-Chanoine, M.H.; Bertrand, X.; Madec, J.Y. Escherichia coli ST131, An intriguing clonal group. Clin. Microbiol. Rev. 2014, 27, 543–574. [Google Scholar] [CrossRef] [Green Version]
  24. Liss, M.A.; Peterson, E.M.; Johnston, B.; Osann, K.; Johnson, J.R. Prevalence of ST131 among fluoroquinolone-resistant Escherichia coli obtained from rectal swabs before transrectal prostate biopsy. Urology. 2013, 81, 548–555. [Google Scholar] [CrossRef] [Green Version]
  25. Manges, A.R.; Geum, H.M.; Guo, A.; Edens, T.J.; Fibke, C.D.; Pitout, J.D.D. Global extraintestinal pathogenic Escherichia coli (ExPEC) lineages. Clin. Microbiol. Rev. 2019, 32, e00135-18. [Google Scholar] [CrossRef]
  26. Johnson, J.R.; Russo, T.A. Extraintestinal pathogenic Escherichia coli: ‘the other bad E. coli’. J. Lab. Clin. Med. 2002, 139, 155–162. [Google Scholar] [CrossRef]
  27. Nataro, J.P.; Kaper, J.B. Diarrheagenic Escherichia coli. Clin. Microbiol. Rev. 1998, 11, 142–201. [Google Scholar] [CrossRef] [Green Version]
  28. Paramita, R.I.; Nelwan, E.J.; Fadilah, F.; Renesteen, E.; Puspandari, N.; Erlina, L. Genome-based characterization of Escherichia coli causing bloodstream infection through next-generation sequencing. PLoS ONE. 2020, 15, e0244358. [Google Scholar] [CrossRef]
  29. Boerlin, P.; McEwen, S.A.; Boerlin-Petzold, F.; Wilson, J.B.; Johnson, R.P.; Gyles, C.L. Associations between virulence factors of Shiga toxin-producing Escherichia coli and disease in humans. J. Clin. Microbiol. 1999, 37, 497–503. [Google Scholar] [CrossRef] [Green Version]
  30. Kaper, J.B.; Nataro, J.P.; Mobley, H.L. Pathogenic Escherichia coli. Nat. Rev. Microbiol. 2004, 2, 123–140. [Google Scholar] [CrossRef]
  31. Kuhnert, P.; Boerlin, P.; Frey, J. Target genes for virulence assessment of Escherichia coli isolates from water, food and the environment. FEMS Microbiol. Rev. 2000, 24, 107–117. [Google Scholar] [CrossRef] [Green Version]
  32. Sarowska, J.; Futoma-Koloch, B.; Jama-Kmiecik, A.; Frej-Madrzak, M.; Ksiazczyk, M.; Bugla-Ploskonska, G.; Choroszy-Krol, I. Virulence factors, prevalence and potential transmission of extraintestinal pathogenic Escherichia coli isolated from different sources: Recent reports. Gut Pathog. 2019, 11, 10. [Google Scholar] [CrossRef] [Green Version]
  33. Williamson, D.A.; Freeman, J.T.; Porter, S.; Roberts, S.; Wiles, S.; Paterson, D.L.; Johnson, J.R. Clinical and molecular correlates of virulence in Escherichia coli causing bloodstream infection following transrectal ultrasound-guided (TRUS) prostate biopsy. J. Antimicrob. Chemother. 2013, 68, 2898–2906. [Google Scholar] [CrossRef]
  34. Czmil, A.; Wronski, M.; Czmil, S.; Sochacka-Pietal, M.; Cmil, M.; Gawor, J.; Wołkowicz, T.; Plewczynski, D.; Strzalka, D.; Pietal, M. NanoForms: An integrated server for processing, analysis and assembly of raw sequencing data of microbial genomes, from Oxford Nanopore technology. Peer J. 2022, 10, e13056. [Google Scholar] [CrossRef]
  35. Larsen, M.V.; Cosentino, S.; Lukjancenko, O.; Saputra, D.; Rasmussen, S.; Hasman, H.; Sicheritz-Pontén, T.; Aarestrup, F.M.; Ussery, D.W.; Lund, O. Benchmarking of methods for genomic taxonomy. J. Clin. Microbiol. 2014, 52, 1529–1539. [Google Scholar] [CrossRef] [Green Version]
  36. Larsen, M.; Cosentino, S.; Rasmussen, S.; Rundsten, C.; Hasman, H.; Marvig, R.; Jelsbak, L.; Sicheritz-Pontén, T.; Ussery, D.; Aarestrup, F.; et al. Multilocus sequence typing of total genome sequenced bacteria. J. Clin. Microbiol. 2012, 50, 1355–1361. [Google Scholar] [CrossRef] [Green Version]
  37. Joensen, K.G.; Tetzschner, A.M.; Iguchi, A.; Aarestrup, F.M.; Scheutz, F. Rapid and easy in silico serotyping of Escherichia coli using whole genome sequencing (WGS) data. J. Clin. Microbiol. 2015, 53, 2410–2426. [Google Scholar] [CrossRef] [Green Version]
  38. Tetzschner, A.M.M.; Johnson, J.R.; Johnston, B.D.; Lund, O.; Scheutz, F. In Silico genotyping of Escherichia coli isolates for extraintestinal virulence genes by use of whole-genome sequencing data. J. Clin. Micobiol. 2020, 58, e01269-20. [Google Scholar]
  39. Bortolaia, V.; Kaas, R.F.; Ruppe, E.; Roberts, M.C.; Schwarz, S.; Cattoir, V.; Philippon, A.; Allesoe, R.L.; Rebelo, A.R.; Florensa, A.R.; et al. ResFinder 4.0 for predictions of phenotypes from genotypes. J. Antimicrob. Chemother. 2020, 75, 3491–3500. [Google Scholar] [CrossRef]
  40. Cosentino, S.; Larsen, M.V.; Aarestrup, F.M.; Lund, O. PathogenFinder—Distinguishing friend from Foe using bacterial whole genome sequence data. PLoS ONE 2013, 8, e77302. [Google Scholar] [CrossRef]
Table 1. Distribution of plasmid-mediated quinolone resistance (PMQRs) determinants among different FQ-resistant phenotypes of 32 E. coli strains isolated from rectal swabs of men undergoing a transrectal prostate biopsy.
Table 1. Distribution of plasmid-mediated quinolone resistance (PMQRs) determinants among different FQ-resistant phenotypes of 32 E. coli strains isolated from rectal swabs of men undergoing a transrectal prostate biopsy.
No.Isolate No.SpeciesResistant to QuinolonesMIC of CIP
PMQRs Genes
1G008E. coliRS0.125qnrB
2A021E. coliRS0.19qnrS
3D025E. coliRS0.19qnrS
4J026E. coliRS0.19qnrB
5G001E. coliRS0.19qnrB, qnrS
6Ł029E. coliRS0.19qnrS
7Ł031E. coliRS0.19qnrS
8A079E. coliRS0.25qnrS
9A083E. coliRS0.25qnrB
10D008E. coliRS0.25qnrS
11F078E. coliRS0.25qnrS
12J006E. coliRS0.25qnrS
13L018 *E. coliRS0.25qnrS
14L047E. coliRS0.25qnrB, qnrS
15B047E. coliRR1,5qnrS
16G021E. coliRR2qnrS
17H015E. coliRR3qnrS
18G019E. coliRR4qnrS
19Ł036 *E. coliRR4qnrB
20H007 *E. coliRR12qnrB
21G022E. coliRR24qnrB, aac(6)-Ib-cr
22G030E. coliRR32qnrB
23G032E. coliRR>32qnrB, aac(6)-Ib-cr
24E005E. coliRR>32aac(6)-Ib-cr
25H038 *E. coliRR>32aac(6)-Ib-cr
26H060E. coliRR>32aac(6)-Ib-cr
27G051E. coliRR>32aac(6)-Ib-cr
28G053E. coliRR>32aac(6)-Ib-cr
29H003E. coliRR>32qnrB
30Ł008E. coliRR>32qnrS
31Ł024E. coliRR>32qnrS
32L044E. coliRR>32qnrS
NA—nalidixic acid, CIP—ciprofloxacin, MIC—minimum inhibitory concentration, *—E. coli strains not subjected to whole genome sequencing (WGS) analysis.
Table 2. The whole genome sequencing (WGS) analysis of 28 PMQR-producing E. coli strains isolated from rectal of men undergoing a transrectal prostate biopsy.
Table 2. The whole genome sequencing (WGS) analysis of 28 PMQR-producing E. coli strains isolated from rectal of men undergoing a transrectal prostate biopsy.
Strain No.SpeciesSerotypeMLSTMIC of CIP
WGS Results
Plasmid ProfileVirulence GenesResistance GenesAmino Acid Changes in:
G008E. coliO15:H-6930.125IncFIA, IncFIBafaA, afaB, afaC, afaD, afaE8, air, chuA, eilA, espP, fyuA, gad, iha, ireA, irp2, iss, iucC, iutA, kpsE, kpsMIII_K96, lpfA, mchB, mchC, mchF, ompT, sitA, terC, traTaph(3′)-Ia, aph(3′′)-Ib, blaTEM-1B, sul2, tet(B), sitABCD, mdf (A)S83L---
A021E. coliO86:H183880.19Col156, IncFIA, IncFIB, IncFIIafaD, chuA, eilA, fyuA, gad, irp2, iss, iucC, iutA, kpsE, kpsMII_K5, senB, sitA, terC, traTant(3′’)-Ia, aph(6)-Id, blaTEM-1B, sul2, tet(B), sitABCDS83L---
D025E. coliO8:H1788740.19Col8282, IncFIB, IncFII, IncX1cia, cvaC, etsC, fyuA, gad, hlyF, iroN, irp2, iss, iucC, iutA, lpfA, mchF, ompT, papC, sitA, terC, traTqnrS1, blaTEM-1B, blaTEM-1C, tetA, sitABCD----
J026E. coliO8:H1782331830.19Col440II, IncFIBcapU, cba, cma, cvaC, fyuA, gad, hlyF, ireA, iroN, irp2, iss, iucC, iutA, kpsMII_K5, mchF, ompT, sitA, terC, tshsitABCD, mdfAS83L---
G001E. coliO117:H4222074660.19IncFIB, IncI2, IncX1, IncYgad, iss, ompT, terCqnrS1, tetA----
Ł029E. coliO55:H4211253020.19IncFIB, ncFII, IncI-1, IncX1cia, fyuA, gad, irp2, iss, lpfA, ompT, terC, traTqnrS1, blaTEM-1B----
Ł031E. coliO8:H25unknown240.19-fyuA, gad, irp2, iss, lpfA, ompT, sitA, terCsitABCDS83L---
A079E. coliO100:H25683210.25IncFIB, IncFII, IncI, IncX1cma; gad; iroN; iss; lpfAqnrS1, aadA1, blaTEM-1B, mdf(A), sul1, tat(A), dfrA1----
A083E. coliO52:H452064unknown0.25Col, Col156, Col8282, IncFIB, IncFICgadqnrB19, mdf(A), tetB----
D008E. coliO60:H202069990.25IncN, IncX4astA, gad, terCqnrS1, aph(3′’)-Ib, aph(6)-Id, sul2--A56T-
F078E. coliO16:H51315060.25IncFIB, IncFIIchuA, fyuA, gad, iha, irp2, kpsE, kpsMII_K5, ompT, papA_F43, senB, terC, traT, yfcVaadA5, aph(3′′)-Ib, aph(6)-Id, dfrA17, sul1, sul2, tet(A),
sitABCD, mph(A), mdf (A),
J006E. coliO8:H1788740.25IncX1fyuA, gad, irp2, iss, lpfA, ompT, papC, terCqnrS1, blaTEM-1B----
L047E. coliO91:H232244790.25IncFIB, IncFII, IncX1, IncFIC(FII), IncI1-I(Alpha)cia, cib, cvaC, etsC, gad, hlyF, iroN, iss, iucC, iutA, lpfA, mchF, ompT, sitA, terC, traT, tshqnrB19, aadA1, aph(3′′)-Ib, aph(6) Id, blaTEM-1B, dfrA1, sitABCD, sul1, sul2, tet(A), floR----
B047E. coliO9:H191622941.5Col8282, IncFII, Inc1-I, IncX4capU, gad, iss, ipfA, ompT, terC, traTqnrS1, blaTEM-1BS83L---
G021E. coliO117:H4428732IncFIB, IncX1, IncFIC (FII)chuA, cma, etsC, fyuA, gad hlyF, hra, ibeA, iroN, irp2, iss, iucC, iutA, kpsE, kpsMII_K5, neuC, ompT, sitA, terC, traT, tsh, usp, vat, yfcVqnrS1, blaTEM-1B, sitABCDS83L---
H015E. coliO117:H4428733IncFIB, IncX1cma; gad; iroN; issqnrS1, blaTEM-1B, mdf(A)S83L---
G019E. coliO33:H4117484IncFIB, IncFIBastA, cea, chuA, etsC, fyuA, gad, hlyF, hra, ireA, iroN, irp2, iss, iucC, iutA, lpfA, ompT, pic, sitA, terC, traT, vatant(3′′)-Ia, blaTEM-84, dfrA1, sul1,
catA1, sitABCD
G022E. coliO33:H2516235524not foundgad; lpfAmdf(A)S83L
G030E. coliO8:H9906632Col440II, IncFIB, IncFIIcma, cvaC, gad, hlyF, iroN, iss, ompT, sitA, terC, traTaadA1, aph(3′′)-Ib, aph(6)-Id, blaTEM-1B, dfrA1, sul1, sul2, tet(A), sitABCD, mdfAS83L
G032E. coliO101:H910unknown>32IncFIB, IncFIIcma, cvaC, gad, hlyF, iroN, iss, ompT, sitA, terC, traTaadA1, aph(3′′)-Ib, aph(6)-Id, blaTEM-1B, dfrA1, sul1, sul2, tet(A), sitABCD, mphBS83L
E005E. coliO25:H413143>32IncFIA, IncFIIgad; iha; iss; nfaE; sataac(6′)-Ib-cr, aadA5, blaCTX-M-15, blaOXA-1, mphA, catB3, sul1, tet(A), dfrA17S83L
H060E. coliO101:H9102>32IncFIA, IncFIB, IncX1gad, iucC, iutA, papC, sitA, terC, traTblaTEM-30, dfrA7, sul1, sul2, tet(B), sitABCD, mdfAS83L
G051E. coliO25:H413143>32Col156, IncFIA, IncFIB, IncFIIchuA, cnf1, fyuA, gad, hra, iha, irp2, iss, iucC, iutA, kpsE, kpsMII_K5, ompT, papA_F43, papC, sat, senB, sitA, terC, traT, usp, yfcVaac(6′)-Ib-cr, blaOXA-1,
sitABCD, catB3
G053E. coliO25:H413143>32Col156, IncFIA, IncFIB, IncFIIcelB, chuA, fyuA, gad, hra, iha, irp2, iss, iucC, iutA, kpsE, kpsMII_K5, ompT, papA_F43, papC, sat, senB, sitA, terC, traT, usp, yfcVaac(6′)-Ib-cr, aadA5, blaCTX-M-15, blaOXA-1, sitABCD, mphA, sul1, catB3S83L
H003E. coliO1:H7951>32IncFIB, IncFIIchuA, cia, cvaC, etsC, fyuA, gad, hlyF, ireA, iroN, irp2, iss, iucC, iutA, kpsE, kpsMII_K1, mchF, neuC, ompT, papA_F11, papC, sitA, terC, traT, usp, vat, yfcVblaTEM-1D, sitABCD, tet(A)S83L-S80I-
Ł008E. coliO9:H1046736>32IncFIB, IncFII, IncX1, IncFIC (FII), IncI1-I(Alpha)cib, cma, cvaC, fyuA, gad, hlyF, iroN, irp2, iss, ompT, sitA, terC, traTqnrS1, aadA1, blaTEM-1B, dfrA15, sitABCD, sul3, tet(A), cmlA1S83L
L024E. coliO9:H1046736>32IncX1fyuA, gad, irp2, terCqnrS1, blaTEM-1B, mdfAS83L
L044E. coliO101:H106172>32IncFIA, IncFIB, IncFII, IncX4, IncNcapU, gad, iss, sitA, terC, traTqnrS1, aadA5, ant(2′′)-Ia, aph(3′′)-Ib, aph(6)-Id, blaTEM-135, blaTEM32, sitABCD, tet(A), tet(B), mdfAS83L
Table 3. Distribution of virulence genes in 28 PMQR-producing E. coli strains isolated from rectal swabs of men undergoing a transrectal prostate biopsy.
Table 3. Distribution of virulence genes in 28 PMQR-producing E. coli strains isolated from rectal swabs of men undergoing a transrectal prostate biopsy.
Virulence FactorVirulence FunctionVirulence
TotalCIP S
MIC ≤ 0.25 mg/L
>0.5 mg/L
Gluta mate decarboxylaseenables the bacteria to survive under acidic conditionsgad281414
Tellurium ion resistance proteininvolved in tellurite resistance by catalysing efflux of tellurium ions;
in complex with TerB protein manages membrane stress response
Increased serum survivalinvolved in resistance process against serum complement system;
the protection factor against phagocytosis
Iron transport proteiniron ion transportsitA710
Outer membrane protease (protein protease 7)confers E. coli resistance to the antimicrobial activity of urinary cationic peptides, including defensinsompT1688
Outer membrane protein complement resistancereduces the sensitivity of E. coli cells to phagocytosis by macrophages;
inhibition of the classical pathway of complement activity
Siderophore receptorferric yersiniabactin uptake receptor FyuA involved in iron-acquisition mechanism;
involved in biofilm formation process in iron-poor environments such as human urine
High molecular weight protein 2 non-ribosomal peptide synthetasemaintains cellular iron homeostasis by regulating the expression of genes involved in iron metabolismirp21486
Aerobactin synthetaseinvolved in siderophore aerobactin synthesisiucC1266
Ferric aerobactin receptoraerobactin iron transport systemiutA1266
Enterobactin siderophore receptor proteinurovirulence factor mediates utilisation of the siderophore enterobactiniroN1147
Hemolysin Finvolved in the increased production of outer membrane vesicles (OMVs), which leads to increased release of toxins such as the cytolethal distending toxin (CDT), cytolysin A (ClyA) and autophagy of infected eukaryotic epithelial cellshlyF1046
Long polar fimbriaeadhesive factors of Shiga toxin-producing E. coli (STEC), associated with colonisation of the intestinelpfA963
Polysialic acid transport protein; Group 2 capsuleinvolved in transport of polysialic acid capsule across the cytoplasmic membrane to the bacteria cell surface
protects from phagocytosis
Outer membrane hemin receptorresponsible for heme uptakechuA835
Colicin Mcytotoxic protein responsible for murein degradation and cell lysis, specifically inhibits murein and O-antigen biosynthesis by interfering with the regeneration of bactoprenolcma835
Capsule polysaccharide export inner-membrane proteininvolved in exporting capsular polysaccharides across the periplasm and outer membrane, which precense facilitate pathogen bacteria evasion of host immune responseskpsE734
Microcin Ckills competitor cells by disrupting the membrane potentialcvaC734
Outer membrane usher P. fimbriaeresponsible for the assembly and secretion of virulence factor, pilus PpapC624
ABC transporter protein MchFinvolved in Mcc, MccH47 siderophore transport outside the producing bacteriamchF651
Putative type I secretion outer membrane proteinefflux transmembrane transporter activityetsC523
Adherence proteinthe most frequently detected adhesins among isolates from UTI patients
probable role in adherence to the epithelial cells in eae-negative STEC strains
Siderophore receptorurovirulence factor, involved in iron acquisitionireA532
Heat-resistant agglutininconfers adherence to eukaryotic cell surfaces and causes bacterial auto-aggregationhra514
Serine protease autotransporters of Enterobacteriaceaecapable of adhering to red blood cells, hemoglobin, extracellular matrix proteins fibronectin and collagen IV
hemagglutination and proteolytic activity
Major pilinenables bacteria to colonise the epithelium of specific host organspapA413
Plasmid-encoded enterotoxininvolved in the development of severe diarrhea in patients infected with Shigella and enteroinvasive E. coli (EIEC)senB422
Uropathogenic specific proteinbacteriocin-like genotoxin
possesses DNase activity, exhibits genotoxic activity in mammalian cells when coapplied with Imu2 protein
provokes DNA damage which leads to apoptosis and ageing of cells
Fimbrial proteinmajor subunit of a putative chaperone-usher fimbriayfcV413
Hexosyltransferase homologprobably responsible for EAEC diarrhea in younger children < 12 monthscapU422
Colicin iainduced by the SOS system during stress
destruction of the cell by forming pores in the affected cell’s cytoplasmic membrane
Serine protease autotransporters of Enterobacteriaceaecleavage of spectrin, induces cytopathic effects on epithelial cellssat303
Colicin ibkills other competitor bacterial strains by pore formation in the inner membranecib211
Polysialic acid capsule biosynthesis proteinan essential enzyme in the biosynthesis of sialic acid, which is a component of E. coli capsuleneuC202
Serine protease autotransporters of Enterobacteriaceaevacuolating autotransporter toxin present in some uropathogenic E. coli (UPEC) strains
induces cellular damage, vacuole formation, urothelial barrier dysregulation of bladder epithelial cells
Afimbrial adhesionmediates the internalisation of adherent bacteria into cellsafaD220
Salmonella HilA homologprobable role in modulation expression of the TTSS and effectors of different chromosomal islands in EAECeilA220
Colicin Bdestroys sensitive bacteria cells by dispersion the membrane potential through channel formationcba220
Heat-stable enterotoxin 1activate guanylate cyclase in the intestinal epithelial cells leading to watery diarrheaastA211
Diffuse adherence fibrillar adhesin geneinvolved in diffuse adherence of E.coli strains to the mucosa of the small intestinenfaE101
Endonuclease colicin E2nuclease activity, involved in cell lysis by degradation of DNA
active under induction of the SOS response by e.g., DNA damage
Cytotoxic necrotizing factorby activating Rho proteins, CNF1 factor provokes actin cytoskeleton rearrangement in the human epithelial cellscnf1101
Invasin of brain endothelial cellscontributes to E. coli K1 invasion of the blood–brain barrieribeA101
Transcriptional regulatorregulates the transcription of genes involved in the biosynthesis of afimbrial adhesin, AfaafA110
Periplasmic chaperoneinvolved in the biogenesis of afimbrial adhesin, AfaafaB110
Outer membrane usher proteinpivotal for virulence factor, Afa adhesins biogenesisafaC110
Adhesin proteinmediates the mannose-resistant hemagglutination (MRHA) of human erythrocytes and specific attachment to epithelial cells by recognition of the decay-accelerating factor (DAF) receptorafaE110
Enteroaggregative immunoglobulin repeat proteinmay promote bacterial aggregation and colonisation in infected hostair110
Putative exoprotein precursorprotease activity, capable to cleaving pepsin A and human coagulationfactor V, which degradation could contribute to the mucosal hemorrhageespP110
Microcin H47 part of colicin Hprecursor peptide of the microcin H47, which impairs the cellular proton channel in the target cellsmchB110
MchC proteininvolved in microcin H47 biosynthesismchC110
Colicin E1leading to death of other E.coli cells by forming pores on the inner membranecea101
Serine protease autotransporters of Enterobacteriaceaeautotransporter secreted by EAEC and other E. coli pathotypes;
mucus secretagogue capability and mucinolytic activity in human goblet cells which secrete MUC2 and MUC5AC
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Piekarska, K.; Zacharczuk, K.; Wołkowicz, T.; Gierczyński, R. Prevalence of Plasmid-Mediated Quinolone Resistance (PMQRs) Determinants and Whole Genome Sequence Screening of PMQR-Producing E. coli Isolated from Men Undergoing a Transrectal Prostate Biopsy. Int. J. Mol. Sci. 2022, 23, 8907.

AMA Style

Piekarska K, Zacharczuk K, Wołkowicz T, Gierczyński R. Prevalence of Plasmid-Mediated Quinolone Resistance (PMQRs) Determinants and Whole Genome Sequence Screening of PMQR-Producing E. coli Isolated from Men Undergoing a Transrectal Prostate Biopsy. International Journal of Molecular Sciences. 2022; 23(16):8907.

Chicago/Turabian Style

Piekarska, Katarzyna, Katarzyna Zacharczuk, Tomasz Wołkowicz, and Rafał Gierczyński. 2022. "Prevalence of Plasmid-Mediated Quinolone Resistance (PMQRs) Determinants and Whole Genome Sequence Screening of PMQR-Producing E. coli Isolated from Men Undergoing a Transrectal Prostate Biopsy" International Journal of Molecular Sciences 23, no. 16: 8907.

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