Articles

Platinum Priority – Infections
Editorial by Riccardo Bartoletti and Tommaso Cai on pp. 528–529 of this issue

Infective Complications After Prostate Biopsy: Outcome of the Global Prevalence Study of Infections in Urology (GPIU) 2010 and 2011, A Prospective Multinational Multicentre Prostate Biopsy Study eulogo1

By: Florian M.E. Wagenlehner a lowast , Edgar van Oostrum b , Peter Tenke c , Zafer Tandogdu d , Mete Çek e , Magnus Grabe f , Björn Wullt g , Robert Pickard h , Kurt G. Naber i , Adrian Pilatz a , Wolfgang Weidner a and Truls E. Bjerklund-Johansen j on behalf of the GPIU investigators.

European Urology, Volume 63 Issue 1, March 2013, Pages 521-527

Published online: 01 March 2013

Keywords: Prostate biopsy, Infective complications, Urinary tract infection, Antibiotic resistance

Abstract Full Text Full Text PDF (145 KB)

Abstract

Background

Infection is a serious adverse effect of prostate biopsy (P-Bx), and recent reports suggest an increasing incidence.

Objective

The aim of this multinational multicentre study was to evaluate prospectively the incidence of infective complications after P-Bx and identify risk factors.

Design, setting, and participants

The study was performed as an adjunct to the Global Prevalence Study of Infections in Urology (GPIU) during 2010 and 2011. Men undergoing P-Bx in participating centres during the 2-wk period commencing on the GPIU study census day were eligible.

Outcome measurements and statistical analysis

Baseline data were collected and men were questioned regarding infective complications at 2 wk following their biopsy. The Fisher exact test, Student t test, Mann-Whitney U test, and multivariate regression analysis were used for data analysis.

Results and limitations

A total of 702 men from 84 GPIU participating centres worldwide were included. Antibiotic prophylaxis was administered prior to biopsy in 98.2% of men predominantly using a fluoroquinolone (92.5%). Outcome data were available for 521 men (74%). Symptomatic urinary tract infection (UTI) was seen in 27 men (5.2%), which was febrile in 18 (3.5%) and required hospitalisation in 16 (3.1%). Multivariate analysis did not identify any patient subgroups at a significantly higher risk of infection after P-Bx. Causative organisms were isolated in 10 cases (37%) with 6 resistant to fluoroquinolones. The small sample size per participating site and in compared with other studies may have limited the conclusions from our study.

Conclusions

Infective complications after transrectal P-Bx are important because of the associated patient morbidity. Despite antibiotic prophylaxis, 5% of men will experience an infective complication, but none of the possible factors we examined appeared to increase this risk. Our study confirms a high incidence of fluoroquinolone resistance in causative bacteria.

Take Home Message

This study prospectively confirmed that infective complications after prostate biopsy have become an important health problem that causes significant morbidity and hospitalizations annually worldwide. The major risk factor for infective complications after prostate biopsy was the fluoroquinolone resistance of causative bacteria.

Keywords: Prostate biopsy, Infective complications, Urinary tract infection, Antibiotic resistance.

1. Introduction

Prostate biopsy (P-Bx) is currently an essential procedure for prostate cancer diagnosis [1] and a frequently performed procedure in urology with an estimated 1 million cases each year in Europe. Following the introduction of transrectal ultrasound-guided P-Bx [2] , this procedure has been widely accepted and optimised in recent years, continuously following the transrectal route [1] . A systematic review on randomised controlled studies (RCTs) on antibiotic prophylaxis in transrectal P-Bx showed a significant reduction in the risk of bacteriuria compared with placebo [3] . Reductions in symptomatic urinary tract infections (UTIs) and bacteremia were also seen but did not reach statistical significance [3] . Clinical guidelines therefore recommend antibiotic prophylaxis, typically with a oral fluoroquinolone, prior to transrectal P-Bx [4] and [5]. Several reports have recently suggested an increased rate of infective complications following transrectal P-Bx in both North America [6] and [7] and Europe [8] . The reasons for this increase and the factors associated with a higher susceptibility to infection remain largely unknown.

The aim of this international study was to evaluate the worldwide prevalence of infective complications after P-Bx and determine whether putative risk factors are associated with a higher rate of infection.

2. Material and methods

2.1. Study design

This prospective observational multinational multicentre epidemiologic study was performed as a part of the annual worldwide Global Prevalence Study on Infections in Urology (GPIU) in 2010 and 2011. The GPIU study has been performed annually since 2003 and consists of a 1-d prevalence census of infections experienced by patients hospitalised in urology units. It is organised by the board of the European Section for Infections in Urology (ESIU) [9] and [10]. The study was endorsed and sponsored by the European Association of Urology (EAU) and carried out in collaboration with several other medical societies (see acknowledgements). The GPIU study was approved by the ethics committee of Justus-Liebig-University, Giessen, Germany (ethical vote: AZ: 116/07). Obtaining regulatory approval was the responsibility of each study centre.

The aims of the GPIU prostate biopsy study were (1) to audit the prevalence of infective complications after P-Bx across centres and countries participating in the GPIU study and (2) to evaluate factors associated with a higher risk of infective complications.

All patients undergoing P-Bx during the 2-wk period commencing on the GPIU study census day in November 2010 and 2011 onwards were eligible to be included. Each included participant was required to be observed for 2 wk after biopsy either by onsite investigation or telephone interview.

2.2. Internet portal

The study was performed using the Internet-based platform Uroweb, the Internet portal of the EAU that provides all protocol details and uploading of results to a patient database. The software was developed (v.0.9) in PHP (a recursive acronym for PHP Hypertext Preprocessor). For the P-Bx study, investigators at participating sites completed online case report forms on a password-protected Web site with a site-specific login ( http://www.uroweb.org/ ). These anonymised data were stored securely in a specially designed MySQL database [9] and [10].

2.3. Patient information

The case report form consisted of two parts. The first part included questions on patient characteristics (age, use of antibiotics in preceding 6 mo, history of urogenital infection in preceding 6 mo, prostate volume, prostate-specific antigen [PSA] value, previous biopsy) and the biopsy process (route, result of preoperative urine culture, performance and type of preoperative bowel preparation, performance and type of antibiotic prophylaxis, number of cores taken, performance of local anaesthesia). The second part comprised questions on the outcome of biopsy (presence of histopathologic inflammation, presence and severity of symptoms of UTI at any time up to 2 wk after biopsy, physician visit for UTI and type of visit, readmission to the hospital, results of urine culture and inflammatory markers, type of treatment antibiotic used, and final clinical outcome at follow-up date).

To assess factors for increased infective complications after P-Bx, patients with infective complications were compared with patients without infective complications with regard to possible adverse risk factors of increasing age, higher prostate volume, higher preoperative PSA level, past history of UTI, and prebiopsy bacteriuria in patients investigated with urine culture, preoperative bowel preparation, history of antibiotic pretreatment, performance of antibiotic prophylaxis, type of antibiotic prophylaxis, duration of antibiotic prophylaxis, repeated P-Bx, use of local anaesthesia at P-Bx, number of biopsy cores, and histopathologic presence of inflammation in the biopsies.

2.4. Statistics

Dichotomous variables were compared with the two-sided Fisher exact test and continuous variables with the two-sided unpaired Student t test or Mann-Whitney U test, where appropriate. A binary logistic regression analysis was used to examine the association between possible predictive factors for the occurrence of a UTI after P-Bx. Missing values were not imputed in the model. We did not include the variables prostate volume or presence of preoperative bacteriuria in the multivariate analytical model because they were recorded for less than half of the cohort. An α value of 0.05 was determined to be statistically significant. Statistical analyses were performed using PASW Statistics 20 for Windows (SPSS GmbH Software, Munich, Germany).

3. Results

A total of 84 centres in Africa (n = 2), Asia (n = 11), Europe (n = 67), and South-America (n = 4) participated in the GPIU prostate biopsy study (see appendix). The centres included a median of 4 evaluable patients for each year of participation (range: 1–25; standard deviation [SD]: ±6.7). A total of 702 men were included across the two study years (2010, n = 385; 2011, n = 317). Median patient age was 66 yr (range: 40–90; SD: ±8.0). Table 1 shows the biopsy performance parameters.

Table 1 Evaluation of prostate biopsy performance in 702 men

Parameter Patients, no. (%)
Urine examination prior to biopsy 418/702 (59.5)
- Reagent strip urinalysis 254/702 (36.2)
- Urine culture * 164/702 (23.4)
Antibiotic treatment for bacteriuria prior to biopsy 2/702 (0.3)
Lower bowel cleansing 297/702 (42.3)
- Enema 246/702 (35.0)
- Antiseptic lavage 25/702 (3.6)
- Other 26/702 (3.7)
Repeat set of biopsies 151/702 (21.5)
Antibiotic prophylaxis 689/702 (98.2)
- Fluoroquinolone-based antibiotic prophylaxis 637/702 (90.8)
Transrectal prostate biopsy § 684/702 (97.4)
Transperineal prostate biopsy § 18/702 (2.6)

* Bacteriuria was found in 8 of 164 patients (4.9%): Escherichia coli, n = 2; Klebsiella species, n = 2; Pseudomonas species, n = 1; Staphylococcus epidermidis, n= 1; Enterococcus species, n = 1; Candida parapsilosis, n = 1.

Second set, n = 106; third set, n = 31; fourth set, n = 7; fifth set, n = 3; seventh set, n = 2; unknown sequence, n = 2.

Duration of antibiotic prophylaxis was a median of 3 d (range: 1–21; standard deviation [SD]: ±2.5).

§ A median of 12 biopsy cores (range: 1–40; SD: ±3.9) were obtained per patient.

Outcome at 2 wk was available for 521 of 702 men (74.2%) (2010, n = 290; 2011, n = 231) ( Table 2 ). Symptomatic UTIs were recorded in 27 of 521 patients (5.2%), with dysuria (n = 19), frequency (n = 18), urgency (n = 10), and prostate pain (n = 9) the most frequent symptoms. Urine culture was positive in 10 of 27 cases (Escherichia coli, n = 8; Pseudomonas species, n = 1; Klebsiella species, n = 1). Fluoroquinolone resistance was observed in 6 of 10 isolates. Febrile UTIs were present in 18 of 521 patients (3.5%), and 16 of 521 patients (3.1%) required hospitalisation due to infection. This included one patient admitted to the intensive care unit with uroseptic shock 1 d after P-Bx. In two men the infection had not resolved by the end of the 2-wk follow-up period. A total of 494 of 521 men (94.8%) showed no evidence of infective complications at up to 2 wk after biopsy. Symptomatic UTI was reported in 1 of the 2 patients submitted by centres in Africa, 3 of 57 submissions (5.3%) from centres in Asia, 21 of 441 submissions (4.8%) from European centres, and 2 of 21 submission (9.5%) from centres in South America. There was no statistical significant difference (p = 0.282) comparing infectious complications from Europe versus Africa, Asia, and South America.

Table 2 Evaluation of possible risk factors comparing patients with versus without symptomatic urinary tract infections

Parameter n Symptomatic UTI (%) No symptomatic UTI (%) p value
Total 521 27/521 (5.2) 494/521 (94.8) NA
Age, yr, median 521 66 67 0.411
Prostate size, ml, median 236 52 46 0.733
PSA, ng/ml, median 501 8 8 0.921
History of UTI 485 0/24 (0) 34/461 (7.4) 0.399
Preoperative bacteriuria * 130 0/9 (0) 5/121 (4.1) 1.000
Preoperative bowel preparation 521 12/27 (44.4) 186/494 (37.7) 0.543
History of antibiotic pretreatment 462 1/21 (4.8) 56/441 (12.7) 0.495
Antibiotic prophylaxis 518 27/27 (100) 484/491 (98.6) 1.000
Fluoroquinolone-based antibiotic prophylaxis 511 23/27 (85.2) 447/484 (92.4) 0.260
Antibiotic prophylaxis >1 d 511 18/27 (66.7) 327/484 (67.6) 1.000
Repeated P-Bx 516 8/25 (32.0) 100/491 (20.4) 0.204
Local anesthesia used 521 15/27 (55.6) 254/494 (51.4) 0.698
No. of biopsy cores, median 521 10 12 0.007
Histopathologic inflammation 448 5/21 (23.8) 140/427 (32.8) 0.479

* In patients where urine culture was performed prior to prostate biopsy.

UTI = urinary tract infection; NA = not applicable; PSA = prostate-specific antigen; P-Bx = prostate biopsy.

To assess factors for increased infectious complications after P-Bx, patients with infectious complications (n = 27) were compared with patients without infectious complications (n = 494) ( Table 2 ). In multivariate analysis no significant association between UTI and any investigated variable was found (for all variables p > 0.05).

4. Discussion

Millions of men undergo P-Bx throughout the world each year as part of the accepted diagnostic pathway for prostate cancer [6] . Recently retrospective studies from Canada [7] and the United States [6] and one prospectively performed study from Europe [8] reported an apparent increase in the incidence of infective complications after transrectal P-Bx. In this study we found that just over 5% of men experienced symptomatic UTI after P-Bx, which resulted in serious morbidity in about 70% of cases with systemic symptoms and admission to hospitals. The rate of systemic infection found in our study is higher than earlier reports in the literature where a rate of 1% was quoted in one large study [11] . This finding is important because the low specificity of PSA testing means that cancer detection rates for initial P-Bx range between 22.8% and 42.0% [1] . A diagnostic procedure with a generally <50% positive detection rate should be as safe as possible.

EAU guidelines classify transrectal P-Bx as a contaminated procedure and, if a urinary catheter or bacteriuria is present, as a dirty procedure [12] warranting antibiotic prophylaxis in all patients. Systematic review and meta-analysis of RCTs confirm that prophylaxis reduces the rate of bacteriuria following P-Bx, although the results for more clinically oriented outcomes such as symptomatic UTI are less certain [3] . These studies have so far focused on the use of fluoroquinolones and trimethoprim/sulfamethoxazole as suitable antibiotics for prophylaxis [3] . This is in line with pharmacokinetic studies in prostate tissue and prostatic secretions that confirm most orally administered fluoroquinolones achieve concentrations in the prostate that should be sufficient for the treatment of chronic bacterial prostatitis caused by susceptible pathogens [13] . High prostatic antibiotic concentrations are equally important in the prophylaxis of P-Bx. The superiority of fluoroquinolones was suggested by the results of a clinical pharmacokinetic study comparing ciprofloxacin (moderate prostatic tissue penetration) versus gentamicin (low prostatic tissue penetration) in prophylaxis against bacteremia following transrectal P-Bx. The study found that use of ciprofloxacin was associated with a lower incidence of bacteremia and clinical bloodstream infection, and this response correlated with higher prostate tissue levels of the drug [14] . There is as yet no consensus on the optimal duration of antibiotic prophylaxis for P-Bx. Our multinational study showed a median duration of 3 d, but there was no association between durations >1 d and the incidence of symptomatic UTI. EAU guidelines recommend single-dose prophylaxis for low-risk patients and prolonged courses of prophylaxis only in high-risk patients [5] ; American Urological Association guidelines generally recommend prophylaxis for <24 h [4] . Because most men undergoing P-Bx are likely to have low levels of comorbidity, reducing the prophylaxis regimens to a single appropriately administered dose as recommended by the EAU guidelines would seem reasonable. This is important as part of the worldwide drive to reduce antibiotic selection pressure and thus decrease the emergence of antibiotic resistance.

Procedure-specific factors for a higher risk of infective complications after P-Bx are still not well defined, and our study was unable to add any further clarity on this issue [12] . It would seem appropriate to check a midstream urine culture prior to the procedure to rule out asymptomatic bacteriuria, which is recommended in the EAU guideline [5] . It is also recommended that in the presence of asymptomatic bacteriuria the prophylactic antibiotic regimen should include an agent tested susceptible to cover the urinary bacteria [5] . In our study, recommended preoperative patient evaluation by urine culture prior to biopsy [5] was performed in only 164 of 702 patients (23.4%) ( Table 1 ). Adherence to guidelines could certainly be improved in this respect.

All other evaluated possible factors for increased infective complications were not significantly different between patients having symptomatic UTI and those who did not; however, diabetes as a risk factor was not investigated in this study. In a previous study it was found that a larger prostate and diabetes were significantly associated with infective complications after P-Bx [8] .

The observational epidemiologic design of our study collecting data at two time points in 2 yr prevented us from looking at changing patterns of infective complications and bacterial resistance over time. Further data collections at annual intervals over the coming years will allow us to achieve this goal. Our study also had insufficient power to be certain of identifying whether or not some of the risk factors examined were associated with the incidence of symptomatic UTI. The small sample size per participating site and in comparison with other studies therefore may have limited the conclusions from our study. Possible risk factors evaluating comorbidities such as diabetes, steroid use, or heart disease have not been evaluated, which is a limitation and will be taken up in subsequent study years. Our data on bacterial isolates do provide provisional support for the faecal carriage of fluoroquinolone-resistant bacteria as a risk factor for infective complications. A previous prospective study in consecutive patients undergoing P-Bx found that 22.0% of patients harboured ciprofloxacin-resistant E coli strains [15] . The study also found that faecal carriage of fluoroquinolone-resistant E coli strains was a significant risk factor for infective complications after P-Bx [15] . Specific fluoroquinolone-resistant E coli strains (eg, E coli ST131) could be detected as an important cause of sepsis after P-Bx [16] . It has also been shown that faecal fluoroquinolone-resistant E coli can even be selected by a single oral dose of 500 mg ciprofloxacin given for the prophylaxis of transrectal P-Bx [17] . The use of fluoroquinolones in the 6 mo before biopsy was also shown to be associated with an increased risk of faecal carriage of fluoroquinolone-resistant E coli strains [15] . Our study adds further credence to the emerging possibility that faecal carriage of fluoroquinolone-resistant E coli strains represents a significant risk factor classifying patients into a high-risk group for infective complications after P-Bx, particularly if, as seems likely, fluoroquinolones remain the most frequently used agents for prophylaxis. The rate of fluoroquinolone resistance amongst isolates from men with symptomatic UTI after P-Bx in the present study was particularly high (60%) compared with rates seen in other hospital settings that ranged from 22.7% to 30.8% [18] . Faecal fluoroquinolone-resistant bacteria as a risk factor could certainly explain the increase of infective complications after P-Bx, paralleling the worldwide increase of fluoroquinolone resistance in enterobacteria [10], [19], and [20].

Strategies capable of decreasing infective complications after P-Bx must therefore be developed and evaluated so as not to dissuade healthy men who would benefit from early prostate cancer management from undergoing P-Bx when clinically indicated. Several strategies are currently debated, such as risk assessment to select patients at higher risk for infective complications, such as microbiological sampling of the faecal flora prior to biopsy to identify susceptibility to specific agents [21] , change of biopsy route (eg, perineal P-Bx), and the evaluation of alternative antibiotics with improved susceptibility to be used for prophylaxis [22] . Antibiotic susceptibility is only one of the criteria for recommending an alternative antibiotic. The pharmacokinetic distribution of the antibiotic within the prostate is equally important, as well as the suitability for this indication demonstrated in a clinical trial.

5. Conclusions

In this prospective multinational study on infective complications after P-Bx, a significant rate of infective complications after P-Bx was observed to be present worldwide. Our study supports the findings of others in suggesting that the presence of faecal fluoroquinolone-resistant bacteria is the most important risk factor. If this is the case, strategies to identify fluoroquinolone-resistant bacteria should be sought so as to decrease infective complications after P-Bx. This important and yearly performed ongoing study will deliver more data in the future and thus be able to address some of these important issues using a global perspective.


Author contributions: Florian M.E. Wagenlehner had full access to all the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis.

Study concept and design: Wagenlehner, van Oostrum, Çek, Naber, Bjerklund-Johansen.

Acquisition of data: Wagenlehner, van Oostrum, Çek, Grabe, Tandogdu, Tenke, Naber, Bjerklund-Johansen.

Analysis and interpretation of data: Wagenlehner, van Oostrum, Çek, Grabe, Tandogdu, Tenke, Pickard, Wullt, Pilatz, Weidner, Naber, Bjerklund-Johansen.

Drafting of the manuscript: Wagenlehner.

Critical revision of the manuscript for important intellectual content: Wagenlehner, van Oostrum, Çek, Grabe, Tandogdu, Tenke, Pickard, Wullt, Weidner, Naber, Bjerklund-Johansen.

Statistical analysis: Wagenlehner, van Oostrum, Pilatz.

Obtaining funding: Wagenlehner, van Oostrum, Çek, Grabe, Tenke, Naber, Bjerklund-Johansen.

Administrative, technical, or material support: van Oostrum.

Supervision: Wagenlehner, Naber, Bjerklund-Johansen.

Other (specify): None.

Financial disclosures: Florian M.E. Wagenlehner certifies that all conflicts of interest, including specific financial interests and relationships and affiliations relevant to the subject matter or materials discussed in the manuscript (eg, employment/affiliation, grants or funding, consultancies, honoraria, stock ownership or options, expert testimony, royalties, or patents filed, received, or pending), are the following: None.

Funding/Support and role of the sponsor: This study was organised by the board of the ESIU and endorsed and sponsored by the EAU and performed in collaboration with the Asian Association of UTI and STD, the International Society of Chemotherapy for Infection and Cancer, and the Interregional Association of Clinical Microbiology and Antimicrobial Chemotherapy.

Acknowledgement statement: The GPIU study group is most grateful to the altruistic contributions of the GPIU investigators (see appendix).

Appendix. Participants in the 2010 and/or 2011 prostate biopsy Global Prevalence Study of Infections in Urology

Patients, n Geographic region Country City Center Investigators
2010 2011
1   Africa Egypt Alzahraa Alzahraa University Hospital Khaled Abdul Moneim
4   Africa Egypt Cairo Ahmed Maher Teaching Hospital Alaa Ahmed Hussein
  2 Asia China Changchun The First Bethune Hospital, Jilin University Yaowen Fu
12   Asia Iran Tehran Hasheminejad Kidney Center Reza Aghelnezhad
  2 Asia Japan Kitakyushu University Hospital of Occupational and Environmental Health Ryoichi Hamasuna
  1 Asia Japan Okayama Okayama University Hospital Koichiro Wada
18 11 Asia Singapore Singapore National University Hospital Fiona Mei Wen Wu
10 5 Asia South Korea Daejeon Chungnam National University Hospital Yong Gil Na
1   Asia South Korea Gwang-Ju Chosun University Hospital Seung Baik
2   Asia South Korea Seoul St. Mary Kim Sukju
5 1 Asia South Korea Suwon St. Vincent Hospital Seung-Ju Lee
2   Asia South Korea Uijeongbu Uijeongbu St. Mary's Hospital Chang Hee Han
  3 Asia United Arab Emirates Abu Dhabi PMC Medhat Ahmad Mohammad Elsayed
1   Europe Bosnia-Herzegovina Mostar Regional Medical Center Mostar Mustafa Bazardzanovic
  3 Europe Bosnia-Herzegovina Sarajevo Clinical Center University of Sarajevo Senad Bajramović
  5 Europe Czech Republic Liberec Regional Hospital Liberec Jan Mecl
3   Europe Czech Republic Nachod County Hospital Petr Prosvic
  9 Europe Czech Republic Opava Slezska Nemocnice Roman Stanek
21   Europe Denmark Aarhus Aarhus University Hospital, Skejby Pernille Skjold Kingo
16   Europe Denmark Fredericia Fredericia Hospital, part of Hospital Littlebelt Kim Hovgaard Andreassen
  18 Europe Estonia Tallinn East-Tallinn Central Hospital Aleksei Nelovkov
17   Europe France Suresnes Hospital Foch Cécile Bach and Henry Botto
  1 Europe Germany Brandenburg Städtisches Klinikum Brandenburg GmbH Jacqueline Wicht
1   Europe Germany Burgwedel Großburgwedel (Klinikum Region Hannover) Juliane Fiebich
7   Europe Germany Frankfurt St. Katharinen Krankenhaus Saskia Carmen Morgenstern
2   Europe Germany Gelsenkirchen Bergmannsheil Buer Stephan Miller
3 2 Europe Germany Giessen Justus-Liebig-University András Rusz
  5 Europe Germany Marburg Urological Office Martin Ludwig
1   Europe Germany Sigmaringen General Hospital Sigmaringen Zoltan Varga
  1 Europe Germany Ulm Bundeswehrkrankenhaus Ulm Christian Löhmann
  1 Europe Germany Weiden Klinikum Weiden Bernhard Schwindl
  1 Europe Greece Aeghion Aeghion General Hospital Theodore Voudoukis
18 4 Europe Hungary Budapest Jahn Ferenc South-Pest Peter Tenke
15   Europe Hungary Budapest Uzsoki Hospital András Paczelt
18 22 Europe Hungary Pecz University of Pecz Szántó Árpád
  3 Europe Hungary Szeged Albert Szent-Györgyi Clinical Center Faculty of Medicine Ágnes Rosecker
  9 Europe Hungary Veszprém Veszprém Megyei Csolnoky Ferenc Kórház Nonprofit Zrt Sándor Gécs
  2 Europe Italy Andria Bonomo Memorial Hospital Angelo Guarriello
  13 Europe Italy Bolzano General Hospital of Bolzano Michele Lodde
10 16 Europe Italy Lecco A. Manzoni Alberto Trinchieri
2   Europe Italy Magenta G. Fornaroli - Magenta Sandro Danilo Sandri
4   Europe Italy Perugia University of Perugia Elisabetta Costantini
  3 Europe Italy Rome Gemelli Hospital - Catholic University Medical School Emilio Sacco
2 1 Europe Italy Trento Santa Chiara Hospital Tommaso Cai
4 1 Europe Macedonia Skopje University Clinic of Surgery St. Naum Ohridski Slobodan Petar Ristovski and Maja Sofronievska Glavinov
  23 Europe Netherlands Nieuwegein St. Antonius Hospital  
1   Europe Poland Torun Nicolaus Copernicus City Hospital Przemyslaw Adamczyk
8 11 Europe Portugal Coimbra Centro Hospitalar de Coimbra Bruno Alexandre Guerra and Jorge Pereira
22   Europe Portugal Lisbon Centro Hospitalar de Lisboa - Zona Central, Hospital de São José Catarina Diogo Gameiro
4   Europe Portugal Matosinhos Hospital Pedro Hispano Tiago Pinto Correia
  1 Europe Romania Arad Arad County Hospital Dana Gabriela Negru
  5 Europe Romania Cluj Napoca EndoPlus Christian Nicolae Manea
  1 Europe Russia Moscow Botkin Hospital Lyubov Alexandrovna Sinyakova
1 6 Europe Russia Moscow Moscow City Hospital 50 Andrey Vladimirovich Zaytsev
3   Europe Russia Togliatti Municipal Health Care City Hospital #1 Rinat Khammatov
1   Europe Russia Moscow S.R. Urology Institute Perepanova Sergeevna Tamara
2 2 Europe Russia Ulyanovsk Ulyanovsk State World War Veterans Hospital Anton Maliavin
5   Europe Slovakia Kosice L. Pasteur University Hospital Jaroslav Beck
5   Europe Slovakia Poprad Nemocnica Poprad a.s. Lukas Kocis
  1 Europe Spain Langreo Hospital Valle del Nalón Miguel Alvarez Mugica
  10 Europe Spain Murcia Virgen de la Arrixaca Pedro López Cubillana
18 5 Europe Spain Pamplona Hospital Virgen del Camino Manuel Montesino-Semper
  5 Europe Spain Pamplona Complejo Hospitalario de Navarra Josep Campa
  12 Europe Spain Santa Cruz de Tenerife Hospital Universitario de Canarias David Hernández Hernández
  2 Europe Spain Tudela Hospital Reina Sofia (Tudela) Jose Angel Cuesta-Alcala
16   Europe Sweden Malmö Malmö University Hospital Magnus Grabe
4 1 Europe Switzerland Geneva University Hospital of Geneva Gregory Johann Wirth and Jacques Klein
7 12 Europe Turkey Edirne Trakya University Hospital Ersan Arda
14   Europe Turkey Erciyes Erciyes University Department of Urology Mustafa Sofikerim
  6 Europe Turkey Kocaeli Kocaeli University Faculty of Medicine  
  1 Europe Turkey Kocaeli Kocaeli Universitesi Hastanesi Nazim Mutlu
1   Europe Turkey Konya Selcuk University Meram Medical Faculty Mehmet Kilinc
6 8 Europe Turkey Isparta Suleyman Demirel University School of Medicine Taylan Oksay
1   Europe Turkey Istanbul Istanbul University Cerrahpasa School of Medicine Sinharib Citgez
  4 Europe Turkey Istanbul Istanbul Egitim Ve Araştirma Hastanesi Soner Ulusoy
7   Europe Turkey Istanbul Istanbul Hospital Suleyman Erdinc Unluer
25 25 Europe United Kingdom Edinburgh Western General Hospital Roland Donat
6   Europe United Kingdom Salford Salford Royal Foundation Trust Laura Derbyshire
3 20 Europe United Kingdom Stoke on Trent University Hospital of North Staffordshire Mark Fraser Saxby
  1 Europe Ukraine Donetsk University Clinic Коlesnikov Vladimir Stanislavovich
17   South America Argentina Buenos Aires Hospital Italiano Maria Ines Staneloni
6   South America Argentina Buenos Aires Instituto Quirurgico del Callao-Sanatorio Anchorena Javier David Altclas
2   South America Argentina Salta El Carmen Jose Ignacio Militello
  10 South America Brazil Florianópolis Centro de pesquisas oncologicas de Santa Catarina Flavio Heldwein

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Footnotes

a Department of Urology, Paediatric Urology and Andrology of the Justus-Liebig-University, Giessen, Germany

b EAU Department, Arnhem, The Netherlands

c Department of Urology, Jahn Ferenc South-Pest Hospital, Budapest, Hungary

d Department of Urology, Taksim Teaching Hospital, Istanbul, Turkey

e Department of Urology, Trakya University, Edirne, Turkey

f Department of Urology, Skåne University Hospital, Malmö, Sweden

g Department of Microbiology, Immunology and Glycobiology, Lund, Sweden

h Institute of Cellular Medicine, Newcastle University, Newcastle upon Tyne, UK

i Technical University, Munich, Germany

j Department of Urology, Aarhus University Hospital, Denmark

lowast Corresponding author. Department of Urology, Paediatric Urology and Andrology, Justus-Liebig-University, Giessen, Rudolf-Buchheim-Str. 7, 35385 Giessen, Germany. Tel. +49 641 98544516; Fax: +49 641 98544509.

Please visit www.eu-acme.org/europeanurology to read and answer questions on-line. The EU-ACME credits will then be attributed automatically.

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