Prevalence of ST131 Among Fluoroquinolone-resistant Escherichia coli Obtained From Rectal Swabs Before Transrectal Prostate Biopsy

doi:10.1016/j.urology.2012.10.056

Urology

Volume 81, Issue 3, March 2013, Pages 548-556

https://doi.org/10.1016/j.urology.2012.10.056 Get rights and content

Objective

To identify the prevalence and characteristics of fluoroquinolone-resistant (FQ-R) Escherichia coli ST131 isolates in men undergoing ultrasound-guided transrectal prostate biopsy (TPB).

Materials and Methods

Twenty-seven FQ-R E coli isolates from rectal swabs from 136 men undergoing TPB at 3 institutions in southern California (January 2009 to March 2010), with a focus on repeat biopsy patients, were assessed for E coli phylogenetic group, sequence type ST131 status, extended virulence genotype, pulsed-field gel electrophoresis profile, and antimicrobial susceptibility profile.

Results

ST131 accounted for 70% of the 27 FQ-R pre-TPB E coli rectal isolates, including 82% of those from non-Asians vs 20% from Asians (P = .017). ST131 was associated negatively with prebiopsy enemas and positively with previous TPB. Compared with non-ST131 isolates, the ST131 isolates had a significantly higher prevalence of 4 virulence genes (sat, usp, ompT, and malX), distinctive virulence profiles, and numerically higher virulence scores (median, 12 vs 8), but similar antimicrobial resistance scores. Most rectal ST131 isolates exhibited pulsed-field gel electrophoresis profiles typical of clinical ST131 isolates.

Conclusion

In our locale, the epidemic multidrug-resistant ST131 clonal group accounts for 70% of FQ-R rectal E coli isolates among men undergoing TPB. Such ST131 isolates have distinctive virulence profiles, are extensively antimicrobial-resistant, and are negatively associated with Asian race. Further investigation is needed regarding risk factors for and clinical consequences of colonization with such strains among men undergoing TPB.

Section snippets

Subjects

The present study population of men with pre-TPB FQ-R rectal E coli was identified during a previous screening study that assessed the prevalence of FQ-R E coli among pre-TPB patients.¹⁶ The clinical protocol, inclusion and exclusion criteria, and patient characteristics were reported elsewhere.¹⁶ In brief, after Institutional Review Board approval at each institution and patient informed consent, rectal swabs were obtained from 136 men scheduled to undergo a TPB at 1 of 3 institutions (Long

Patient Characteristics and ST131 Status

Characteristics of the 27 men whose FQ-R pre-TPB rectal E coli isolates were available for analysis are reported in relation to ST131 colonization status in Table 1. The number of FQ-R isolates per subject per institution (% of present study population) was 13 (48%) for Long Beach Veterans Affairs Medical Center, 5 (19%) for Southern California Kaiser Permanente, and 9 (33%) for University of California Irvine Medical Center. There was no difference in whether a 1-day vs 3-day regimen was

Comment

The rectal reservoir is probably the “staging ground” for most urinary tract infections, including those that occur after TPB, in which context the biopsy needle provides rectal microorganisms with direct access to the urinary tract. Unfortunately, intestinal FQ-R E coli have been detected in the pre-TPB population at rates of 10% to 30%, which predictably would predispose TPB recipients to FQ-R E coli infections.6, 13, 16, 21 Indeed, despite fluoroquinolone prophylaxis, the overall post-TPB

Conclusions

Our study found 70% of 27 FQ-R fecal E coli isolates from men undergoing TPB in our locale represented the epidemic multidrug-resistant ST131 clonal group. Compared with non-ST131 isolates, the ST131 isolates exhibited highly distinctive aggregate virulence profiles, a significantly higher prevalence of 4 specific virulence genes (sat, usp, ompT, and malX), and a lower prevalence of cefazolin resistance and ESBL phenotype. ST131 was associated negatively with Asians and prebiopsy sodium

Acknowledgments

The manuscript is dedicated to Amy Nakama-Peeples, who performed most of the isolation and sensitivity analysis in the microbiology lab and tragically passed away; she will be missed dearly. Drs. Richard Szabo (Southern California Kaiser Permanente) and Atreya Dash (Long Beach Veterans Affairs Medical Center and University of California-Irvine Medical Center) helped obtain Institutional Review Board approval and participated in initial patient enrollment at the respective institutions.

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Cited by (29)

Molecular genetic testing does not improve the detection of fluoroquinolone resistance before transrectal prostate biopsy
2022, Prostate International
Citation Excerpt :
One alternate approach is to use next-generation sequencing to identify quinolone resistance (PCR Screen). Our group identified a strain of E. coli (sequence type 131) as a causal source in more than 70% of the infections that occur post-TPB.13,14 Plasmids are another mechanism bacteria used to share genetic information to survive antibiotic exposures but have not been thoroughly evaluated.15
Fluoroquinolone-resistant (FQR) Escherichia coli (E. coli) causes transrectal prostate biopsy infections. We seek to further identify fluoroquinolones resistance by the incorporation of genetic profiling to influence antibiotic selection for transrectal prostate biopsy and whether the addition of this genetic testing could improve the prediction of FQR detection at the time of biopsy.
In this prospective observational cohort study, rectal swabs were collected within 30 days of an upcoming prostate biopsy. These swabs were sent for phenotypic and genotypic assessment to predict FQR on the day of the biopsy. Phenotype: Specimens were inoculated onto MacConkey agar containing ciprofloxacin using standard culture techniques to determine FQR status. Genotype: We compared cultures to polymerase chain reaction (PCR) sequence typing (E.coli- ST131/H30/ST69) and bacterial plasmids (gyrA, qnrQ, and qnrS). The presence of FQR on this testing was compared to the second rectal swab collected just before biopsy (2 hours after ciprofloxacin prophylaxis), which served as the gold standard for FQR.
Overall, the FQR rate was 23.6%. The bacterial plasmids (qnr) were present in 54.1% of samples, and multidrug-resistant E. coli ST131 was present in 12.5% of samples. In comparison, phenotypic assessment using rectal culture had a better prediction for the presence of FQR as compared to genotypic testing [area under the curve (AUC) = 0.85 in phenotype arm vs. AUC = 0.45 in genotype arm].
We detected a high prevalence of FQR genes in the rectum, but the addition of PCR-based genotyping did not improve the prediction of culture-based FQR at the time of biopsy.
Phylogenetic and antibiotics resistance in extended-spectrum B-lactamase (ESBL) Uropathogenic Escherichia coli: An update review
2021, Gene Reports
Escherichia coli (E. coli) is one of the normal flora of human intestine as well as most animals. E. coli can cause numbers of intestinal and extra-intestinal disorders, including urinary tract infections, diarrhea, neonatal meningitis, and septicaemia. In the worldwide, more than 150 million new urinary tract infection (UTI) are detected annually and Uropathogenic E. coli (UPEC), a member of extra-intestinal pathogenic E. coli (EXPEC) group, is associated with approximately 80% of all UTIs. UTI is a typical of infection that is caused by extended-spectrum B-lactamase (ESBL)-producing Enterobacteriaceae (ESBL-PE). Altered genotype, and consequently phenotype, potentiated detecting of various ESBL-producing UPEC strains that can provide development of new therapeutic options using various antibiotics. In this review, we have evaluated recent studies about expression of different genes and phylogenetics of strains from ESBL-UPEC and resistance or sensitivity of these strains versus the antibiotics.
Effect of Augmented Antimicrobial Prophylaxis and Rectal Swab Culture–guided Targeted Prophylaxis on the Risk of Sepsis Following Transrectal Prostate Biopsy
2020, European Urology Focus
Sepsis is a severe complication following transrectal ultrasound-guided prostate biopsy (TRUSPBx). Ciprofloxacin is commonly used for prophylaxis; however, there is an increasing incidence of resistant enteric organisms worldwide.
To investigate the effect of a targeted prophylactic antimicrobial regimen based on rectal swab cultures in reducing the rate of sepsis.
A total of 1012 patients were included. Group A (609 patients) received an empirical prophylactic antimicrobial regimen of gentamicin, metronidazole, and ciprofloxacin. Targeted antimicrobial prophylaxis was introduced due to significant ciprofloxacin and gentamicin resistance in patients admitted with sepsis following TRUSPBx. The remaining 403 patients (Group B) had rectal swab cultures performed prior to biopsy. Patients with organisms resistant to ciprofloxacin or gentamicin received a targeted prophylaxis regimen of fosfomycin, amikacin, and metronidazole.
We retrospectively collected and analysed data on sepsis and bacteraemia for all patients as well as data on rectal swab culture, recent foreign travel, and recent antibiotic use for patients in Group B.
In group A, 12 (2.0%) patients developed sepsis following TRUSPBx, while in group B, 9 (2.2%) patients developed sepsis despite targeted prophylaxis (p = 0.82). Patients with ciprofloxacin-resistant rectal flora had a significantly higher rate of sepsis (9.1% vs 1.1%; p = 0.003). There was a reduction in patients admitted with bacteraemia and severe sepsis between group A (1.2%) and group B (0.3%) which did not reach statistical significance (p = 0.16). In group B, 55 of 403 (13.6%) patients had ciprofloxacin-resistant rectal flora, while 66 (16.4%) had organisms resistant to both ciprofloxacin and gentamicin. A recent foreign travel history was associated with an increased incidence of ciprofloxacin-resistant rectal flora (23.6% vs 10.8%; p = 0.007). The main limitations of our study include its retrospective nature and potential under-reporting of less severe infectious complications.
Rectal swab cultures identify patients with ciprofloxacin-resistant rectal flora who have an eight-fold risk of sepsis. Targeted antimicrobial prophylaxis may not be beneficial in reducing the sepsis rate when compared with augmented empirical prophylaxis. In an era of increasing antimicrobial resistance, transperineal prostate biopsies should be considered to reduce the risk of infective complications.
Performing rectal swab culture prior to transrectal prostate biopsy can help identify patients at risk of developing sepsis despite targeted prophylactic antibiotics.
Prospective Implementation of a Point-of-Care PCR-Based Detection Method to Guide Antibiotic Use Prior to Prostate Biopsy Compared to Targeted Prophylaxis and Physician Choice
2019, Urology
To perform pilot testing regarding implementation of a point-of-care qPCR-based test (EST200) targeting bacterial clonal groups representing the majority of sepsis-causing Escherichia coli before prostate biopsy to determine antibiotic selection.
After IRB approval, we obtained rectal swabs to compare real-time qPCR analysis on a Rotor-Gene Q instrument (Qiagen, Hilden, Germany) to standard culture on ciprofloxacin infused (10mg/L) MacConkey agar and susceptibility testing. Techniques are compared by an area under the receiver operative curve (AUC).
A total of 140 men participated in the study, 102 prebiopsy cultures were utilized to guide prophylaxis. We did not meet our accrual for the randomized portion of the clinical study, yet we did randomized 38 men without prebiopsy cultures to physician choice of antibiotic versus PCR-based approach. Regarding predicting Fluoroquinolone Resistant (FQR) at biopsy, prebiopsy cultures had an AUC of 0.91 (95%CI 0.84-1.00, P > .001) and polymerase chain reaction (PCR) had an AUC of 0.71 (95%CI 0.58-0.84, P = .005) (AUC comparison; Z = 2.31, P = .02). PCR correctly identified 4 of 5 FQR specimens. The PCR test attained an AUC of 0.79 (95%CI 0.56-1.00, P = .044) for detection of total FQR on the day of the biopsy. Risk-based techniques may overcompensate with additional antibiotics (21% versus 0%, P = .10).
EST200 is a rapid PCR-based microbial detection system that has moderate ability to detect total FQR at the time of biopsy. Our study is underpowered, yet provide opportunities to improve the point of care PCR method, such as table tope testing in less than 20 minutes and include additional antibacterial resistant genes.
Rectal culture-directed antibiotic prophylaxis before transrectal prostate biopsy: Reduced infectious complications and healthcare costs
2018, Actas Urologicas Espanolas
La biopsia prostática transrectal ecográficamente dirigida (BPTE) se asocia a complicaciones infecciosas (CI). Las CI están relacionadas con un incremento de la prevalencia de bacterias ciprofloxacino-resistentes (BCR) en la flora rectal. Estudiamos las CI ocurridas en 2 grupos. Grupo de profilaxis antibiótica «dirigida» (GPD) vs. grupo de profilaxis empírica (GPE). Evaluamos el impacto económico que supone la profilaxis antibiótica «dirigida» (PD).
El GPD se estudió prospectivamente (junio 2013-julio 2014). Se recogieron cultivos rectales (CR) antes de BPTE y se sembraron en medios selectivos con ciprofloxacino para determinar la presencia de BCR. Los pacientes con bacterias sensibles recibieron ciprofloxacino. Pacientes con bacterias resistentes recibieron PD según antibiograma del CR.
El GPE se estudió retrospectivamente (enero 2011-junio 2009). El CR no se realizó y todos los pacientes recibieron ciprofloxacino como profilaxis.
Las CI ocurridas en ambos grupos se registraron en un periodo no superior a 30 días después de BPTE (historia clínica electrónica).
Trescientos pacientes fueron sometidos a BPTE, 145 recibieron PD y 155 PE. En el GPD, 23 pacientes (15,86%) presentaron BCR en CR. Solo un paciente (0,7%) experimentó ITU. En el GPE, 26 pacientes (16,8%) experimentaron múltiples CI (incluidas 2 sepsis) (p < 0,005). El coste total estimado, incluido el manejo de las CI, fue de 57.076€ con PE vs. 4.802,33€ con PD. El coste promedio/paciente con PE fue de 368,23€ vs. 33,11€ con PD. La PD logró un ahorro total estimado de 52.273,67€. Es necesario que 6 pacientes se sometan a PD para prevenir una CI.
La PD se asoció a un notable descenso de la incidencia de CI causadas por BCR y redujo los costos de atención sanitaria.
Transrectal ultrasound-guided prostate biopsy (TUPB) is associated with infectious complications (ICs), which are related to a greater prevalence of ciprofloxacin-resistant bacteria (CRB) in rectal flora. We examined the ICs that occurred in 2 groups: A guided antibiotic prophylaxis (GP) group and an empiric prophylaxis (EP) group. We assessed the financial impact of GP.
The GP group was studied prospectively (June 2013 to July 2014). We collected rectal cultures (RCs) before the TUPB, which were seeded on selective media with ciprofloxacin to determine the presence of CRB. The patients with sensitive bacteria were administered ciprofloxacin. Patients with resistant bacteria were administered GP according to the RC antibiogram.
The EP group was studied retrospectively (January 2011 to June 2009). RCs were not performed, and all patients were treated with ciprofloxacin as prophylaxis.
The ICs in both groups were recorded during a period no longer than 30 days following TUPB (electronic medical history).
Three hundred patients underwent TUPB, 145 underwent GP, and 155 underwent EP. In the GP group, 23 patients (15.86%) presented CRB in the RCs. Only one patient (0.7%) experienced a UTI. In the EP group, 26 patients (16.8%) experienced multiple ICs (including 2 cases of sepsis) (P < .005). The estimated total cost, including the management of the ICs, was €57,076 with EP versus €4802.33 with GP. The average cost per patient with EP was €368.23 versus €33.11 with GP. GP achieved an estimated total savings of €52,273.67. Six patients had to undergo GP to prevent an IC.
GP is associated with a marked decrease in the incidence of ICs caused by CRB and reduced healthcare costs.
Trends in Antibiotic Resistance in Urologic Practice
2016, European Urology Focus
Citation Excerpt :
ST131 accounted for 40% of all E. coli bloodstream isolates after TRUPB [76]. Another study reported that 70% of fluoroquinolone-resistant E. coli isolated from rectal swabs taken from men before prostate biopsy belonged to ST131 [88]. The strong association between fluoroquinolones and ESBL production [89] has major implications in the setting of postbiopsy sepsis when considering prophylactic agents before TRUPB.
The significant global upsurge in antimicrobial resistance, particularly among Enterobacteriaceae, represents a serious threat to health care systems. The implications for urologic practice are of particular concern.
To review trends in antibiotic resistance in urologic practice.
We report current European trends of resistance in Gram-negative uropathogens.
In addition to β-lactam resistance, Gram-negative pathogens are often resistant to multiple drug classes, including aminoglycosides, fluoroquinolones, and carbapenems, commonly used to treat urologic infections. Interest is renewed in old antibiotics, and several new antibiotics are in the pipeline to meet the challenge of treating these infections. In this review, we summarise emerging trends in antimicrobial resistance and its impact on urologic practice. We also review current guidelines on the treatment and prevention of urologic infections with these organisms, and some key antibiotics in the era of resistance.
Increasing antimicrobial resistance represents a challenge to urologic practice for both treatment and prophylaxis. Antibiotic choice should be determined according to risk factors for multidrug resistance. Good knowledge of the local microbial prevalence and resistance profile is required to guide antimicrobial therapy.
Antimicrobial resistance represents a challenge in urology. We summarise emerging trends in antimicrobial resistance and review current guidelines on the treatment and prevention of urologic infections, as well as some key antibiotics in the era of resistance.

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: Financial Disclosure: The authors declare that they have no relevant financial interests.

: Funding Support: This material is partly based on work supported by the Office of Research and Development, Medical Research Service, Department of Veterans Affairs, grant #I01 CX000192 01 (J.R.J.). Hardy Diagnostics provided the quality-controlled culture media, and Copan Diagnostics provided the culture swabs.

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Infectious DiseasesPrevalence of ST131 Among Fluoroquinolone-resistant Escherichia coli Obtained From Rectal Swabs Before Transrectal Prostate Biopsy

Objective

Materials and Methods

Results

Conclusion

Section snippets

Subjects

Patient Characteristics and ST131 Status

Comment

Conclusions

Acknowledgments

J Urol

J Urol

J Urol

J Urol

J Urol

Urology

Urology

Eur Urol

J Urol

Urology

Urology

Global cancer statistics

CA Cancer J Clin

Increasing hospital admission rates for urological complications after transrectal ultrasound guided prostate biopsy

J Urol

Infection: prostate biopsy-infection and prior fluoroquinolone exposure

Nat Rev Urol

Infection after transrectal ultrasonography-guided prostate biopsy: increased relative risks after recent international travel or antibiotic use

BJU Int

Infectious Diseases
Prevalence of ST131 Among Fluoroquinolone-resistant Escherichia coli Obtained From Rectal Swabs Before Transrectal Prostate Biopsy