pathogens

Article
The Global Prevalence of Infections in Urology Study:
A Long-Term, Worldwide Surveillance Study on
Urological Infections
Florian Wagenlehner 1, *,† , Zafer Tandogdu 2,† , Riccardo Bartoletti 3 , Tommaso Cai 4 , Mete Cek 5 ,
Ekaterina Kulchavenya 6 , Béla Köves 7 , Kurt Naber 8 , Tamara Perepanova 9 , Peter Tenke 7 ,
Björn Wullt 10 , Florian Bogenhard 11 and Truls Erik Bjerklund Johansen 12
Received: 22 October 2015; Accepted: 13 January 2016; Published: 19 January 2016
Academic Editor: Lawrence S. Young
1 Department of Urology, Paediatric Urology and Andrology, Justus-Liebig-University,
D-35392 Giessen, Germany
2 Northern Institute for Cancer Research, Newcastle University, Newcastle Upon Tyne NE2 4HH, UK;
drzafer@gmail.com
3 Department of Experimental and Clinical medicine, University of Florence, 4-50121 Florence, Italy;
riccardo.bartoletti@unifi.it
4 Department of Urology, Santa Chiara Regional Hospital, 38122 Trento, Italy; ktommy@libero.it
5 Department of Urology, Trakya Medical School, Edirne 22100, Turkey; cekmd@doruk.net.tr
6 TB Research Institute, Novosibirsk 630040, Russia; ku_ekaterina@mail.ru
7 Jahn Ferenc South Pest Teaching Hospital, 1204 Budapest, Hungary; urologia@jahndelpest.hu (B.K.);
tenke.peter@jahndelpest.hu (P.T.)
8 Department of Urology, Technical University of Munich, 80333 Munich, Germany; kurt.naber@nabers.de
9 S.R. Urology Institute, Moscow 105425, Russia; perepanova2003@mail.ru
10 Department of Microbiology, Immunology and Glycobiology, Lund University, 22100 Lund, Sweden;
bjorn.wullt@med.lu.se
11 Department of Bioinformatics, Technische Hochschule Mittelhessen, 35390 Giessen, Germany;
florian.bogenhard@mni.thm.de
12 Department of Urology, Oslo University, 0586 Oslo, Norway; t.e.b.johansen@medisin.uio.no
* Correspondence: wagenlehner@aol.com; Tel.: +49-641-985-44500; Fax: +49-641-985-44509
† These authors contributed equally to this work.

Abstract: The Global Prevalence of Infections in Urology (GPIU) study is a worldwide-performed

point prevalence study intended to create surveillance data on antibiotic resistance, type of urogenital
infections, risk factors and data on antibiotic consumption, specifically in patients at urological
departments with healthcare-associated urogenital infections (HAUTI). Investigators registered data
through a web-based application (http://gpiu.esiu.org/). Data collection includes the practice
and characteristics of the hospital and urology ward. On a certain day in November, each year,
all urological patients present in the urological department at 8:00 a.m. are screened for HAUTI
encompassing their full hospital course from admission to discharge. Apart from the GPIU main study,
several side studies are taking place, dealing with transurethral resection of the prostate, prostate
biopsy, as well as urosepsis. The GPIU study has been annually performed since 2003. Eight-hundred
fifty-six urology units from 70 countries have participated so far, including 27,542 patients. A proxy
for antibiotic consumption is reflected by the application rates used for antibiotic prophylaxis
for urological interventions. Resistance rates of most uropathogens against antibiotics were high,
especially with a note of multidrug resistance. The severity of HAUTI is also increasing, 25% being
urosepsis in recent years.

Keywords: healthcare-associated urinary tract infections; surveillance study; antibiotic resistance;

antibiotic administration; urosepsis; prostate biopsy; transurethral resection

Pathogens 2016, 5, 10; doi:10.3390/pathogens5010010 www.mdpi.com/journal/pathogens

Pathogens 2016, 5, 10

Pathogens 2016, 5, 10 2 of 8

1. Introduction
1. Introduction
Healthcare-associated infections
Healthcare-associated infections (HAI)(HAI) impose
impose aa serious
serious threat
threat onon the
the healthcare
healthcare of of patients
patients in
in
terms of morbidity, as well as mortality. The continued increase of the
terms of morbidity, as well as mortality. The continued increase of the antimicrobial resistance of antimicrobial resistance of
pathogens worldwide
pathogens worldwide is is also
also aa cause
cause of of concern,
concern, since
sincepathogens
pathogensdo donotnotrespect
respectgeographical
geographicalborders.
borders.
The prevalence and outcome of HAI is an important quality parameter
The prevalence and outcome of HAI is an important quality parameter that is routinely collected by that is routinely collected
by monitors
monitors of healthcare
of healthcare in in a numberofofcountries.
a number countries.Reducing
Reducingthe therisk
riskand,
and, hence,
hence, prevalence
prevalence of of
healthcare-associated infections
healthcare-associated infections is is aa key
key priority
priority inin all
all healthcare
healthcare systems,
systems, and and for
for this
this purpose,
purpose, local
local
and international monitoring is
and international monitoring is very useful.very useful.
Healthcare-associated urogenital
Healthcare-associated urogenital tract tract infections
infections (HAUTI)
(HAUTI) are are some
some of of the
the most-frequently
most-frequently
occurring HAI. In a recent U.S.-wide multistate point-prevalence survey,
occurring HAI. In a recent U.S.-wide multistate point-prevalence survey, 12.9% of all HAI 12.9% of all HAI were
weredue to
due
HAUTI [1]. In a European point prevalence survey conducted by the
to HAUTI [1]. In a European point prevalence survey conducted by the European Center for Disease European Center for Disease
Prevention and
Prevention and Control
Control (ECDC),
(ECDC), HAUTIHAUTI accounted
accounted for for 19.0%
19.0% ofof all
all HAI
HAI [2].
[2]. These
Thesefigures,
figures,however,
however,
may vary significantly in different clinical cohorts. Especially, clinical cohorts
may vary significantly in different clinical cohorts. Especially, clinical cohorts with interventions in with interventions in
the urogenital tract are more prone to acquire HAUTI, such as urology. It
the urogenital tract are more prone to acquire HAUTI, such as urology. It is therefore important that is therefore important that
specific surveillance
specific surveillance data data areare generated
generated for for urological
urological patients.
patients. Specific
Specific data
data onon HAUTI
HAUTI in in urology
urology
patients, however, are rare. It was therefore that a prevalence study on infections
patients, however, are rare. It was therefore that a prevalence study on infections in urological in urological patients
was started in 2003 with the aim to deliver surveillance data at the European
patients was started in 2003 with the aim to deliver surveillance data at the European level first level first and was called
and
the Pan European Prevalence (PEP) study. In 2004, the study was enlarged
was called the Pan European Prevalence (PEP) study. In 2004, the study was enlarged to Asia and to Asia and called the Pan
EuroAsian Prevalence (PEAP) study. From 2005 on, the study was run
called the Pan EuroAsian Prevalence (PEAP) study. From 2005 on, the study was run annually and annually and world-wide and
was named and
world-wide the Global
was named Prevalence
the Globalof Infections
Prevalence inofUrology
Infections(GPIU) study (GPIU)
in Urology [3] (Figure
study 1).[3] (Figure 1).

GPIU world
Figure 1. GPIU world map. Participating
Participating countries
countries are marked in red.

The
The primary
primary aims
aims of
of the
the study
study are to do
are to do the
the following
following in
in urology
urology departments
departments throughout
throughout
the world:
the world:

(1) (1) Evaluate

Evaluate urology
urology practice
practice in terms
in terms of hospital
of hospital infection
infection control,
control, whichwhich includes:
includes:
a. Control programs for catheters, antibiotics, etc.;
a Control programs for catheters, antibiotics, etc.;
b. Antibiotic consumption practice.
b Antibiotic consumption practice.
(2) Evaluate UTI and surgical site infections (SSI) in hospitalised urological patients,
(2) Evaluate
whichUTI and surgical site infections (SSI) in hospitalised urological patients, which includes:
includes:
a a.Patient baseline
Patient characteristics;
baseline characteristics;
b Pathogens and their antimicrobial resistance;
2/8
Pathogens 2016, 5, 10 3 of 8

c Antimicrobial treatment.
(3) Determine the prevalence of HAI for:
a Geographical regions;
b Varying hospital setting;
c Study years.

Through these aims, the results of the study will provide national and international data on
UTI and SSI for use in further research and will allow individual institutions to bench-mark their
performance against national and international peers.
The secondary aims of the study are to offer participating urology departments and urologists:

(1) an instrument for quality control of healthcare-associated infections within their institution;
(2) acknowledgement of active involvement in an infection control program (European Section
for Infections in Urology (ESIU)/European Association of Urology (EAU) Certificate for
infection control).

2. Results and Discussion

The initial findings of the PEP and PEAP studies in 2003 and 2004 showed that the prevalence
of HAUTI was 11% in the combined analysis of both initial years [4]. The most frequent forms of
HAUTI were asymptomatic bacteriuria in 29%, followed by cystitis in 26%, pyelonephritis in 21% and
urosepsis in 12% [4]. Especially, the frequency of urosepsis, however, increased significantly over the
last years [5]. This is a worrying figure, also with regard to possible increased mortality, although
the contributing factors are not entirely clear, but might include increased age, higher comorbidities
and more complicated interventions in this patient population. This finding calls for a high level of
awareness in the urological patient population, to note that HAUTI are severe infections, merging into
urosepsis in up to 25% [5].
A total of 56% of the hospitalized urological patients were receiving antimicrobial therapy on
that study day, of whom 46% received antibiotics for prophylaxis, 26% for microbiologically-proven
UTI, 21% for only clinically-suspected UTI and 7% for other infections [6]. The most commonly-used
antibiotics were broad spectrum agents, such as fluoroquinolones in 35%, cephalosporins in 27% and
penicillins in 16%. Differences between countries and regions, however, were highly significant at that
stage [6]. In the follow up studies, a total of 27,542 patients were included in the study on a worldwide
global level until now. Routine antibiotic prophylaxis of all urological procedures was highest in
Asia, Africa and Latin America with 86%, 85% and 84%, followed by Europe with 67%. Antibiotic
prophylaxis was not always consistent with recommended guidelines [7].
Resistance rates of all antibiotics tested other than carbapenems against the total bacterial spectrum
were higher than 10% in all regions. The resistance rates of most of the uropathogens against the
antibiotics tested did not show significant trends of increase or decrease, but were high already in
the beginning years. Resistance to almost all pathogens was lowest in North Europe and highest in
Asia [8].
The studies showed that there was a correlation between increased antibiotic use, often with
broad-spectrum antimicrobials and increased antimicrobial resistance [9]. This finding is in line
with the observations that increased antibiotic consumption, especially of antibiotic agents with the
propensity for collateral damage on the microbiome, leads to antibiotic resistance and multi-resistance.
To interrupt such a vicious cycle, our results suggested that there is room for improvement in surgical
prophylaxis in terms of limiting exposure to antibiotics and that too many patients with asymptomatic
bacteriuria were treated with antibiotics [9]. In addition, a bundle of tools will need to be implemented
to slow down the emergence of resistance, such as antimicrobial stewardship and implementation of
non-antibiotics strategies in benign infections, amongst others.
Pathogens 2016, 5, 10 4 of 8

Emerging data showed that infection is a serious adverse effect of prostate biopsy; therefore,
we performed a prostate biopsy side study with the aim to prospectively evaluate the incidence of
infective complications after prostate biopsy and identify risk factors in the years 2010 and 2011 [10].
In a total of 702 men included from 84 GPIU participating centres worldwide with outcome data
available for 521 men, symptomatic UTI was seen in 5%, febrile UTI in 3.5%, and 3% required
hospitalisation. Multivariate analysis did not identify any patient subgroups at a significantly
higher risk of infection after prostate biopsy. This side study also confirmed a high incidence of
fluoroquinolone resistance in causative bacteria [10].
The detailed results of the side study on TURP will be presented elsewhere.
Given the fact that HAUTI are a significant clinical problem, especially in urology, the rising
antimicrobial resistance calls for a closer monitoring of HAUTI on an international level within
urology [11]. In order to meet these challenges, the ESIU has been performing this prevalence study
with great success for more than 11 years now. It is also a quality improvement initiative related to
HAUTI. The study is able to demonstrate what risk factors are important and how these risk factors
are developing over time. Although the study is a prevalence study, it incorporates some longitudinal
aspects, as patients are evaluated throughout their full hospital course, which resembles a unique
study design, creating valuable data.
The long-term course of the study since 2003 also enabled detecting important emerging issues,
such as infectious complications after prostate biopsy or the fact that the severity of HAUTI has
increased. This led to the development of side studies that explicitly deal with these new emerging
problems, in order to prospectively create data, possibly leading to changes in clinical practice.

3. Experimental Section

3.1. Study Design

The GPIU study is a multinational, multicentre study, performed annually since 2003 as a one-day
prevalence study in November of each year. This time of the year was chosen to have a uniform time
period across the world. The study was initiated and organized by the board of the European Section
for Infections in Urology (ESIU), a section of the European Association of Urology (EAU). The study
was endorsed by the ESIU and sponsored by the EAU. The study is a web-based application, and data
are delivered online. Participating centres provide information regarding their hospital and urology
ward characteristics and practice.

3.2. Study Day Allocation

Each participating department can freely choose a single study day within several listed periods
during November and December of each year. On the chosen single study day at 08:00 a.m. local
time, all patients present in the ward should be screened and included. The presence of UTI and/or
SSI according to the Centers for Disease Control (CDC) definitions during their entire hospital stay
should be documented and audited, encompassing the patients’ full hospital course from admission
to discharge. The investigators have to state for each reported patient whether the infections is
a HAUTI or not. Thus, the charts and case records of the included patients should be examined both
retrospectively and prospectively and patients categorized as having or not having a UTI or SSI. All
uploaded patient information is reported anonymously to the central study file. All participating
departments are allocated their own study page where their patients are listed anonymously according
to subject numbers. Data of the years 2003 and 2004 were combined into one group due to data file
structure changes made in 2005.

3.3. Internet Application

Study-report forms are available through the GPIU portal at http://gpiu.esiu.org/ [12].
Pathogens 2016, 5, 10 5 of 8

An original Internet application has been developed and programmed in PHP (a recursive
Pathogens 2016, 5, 10
acronym for PHP Hypertext Preprocessor). The structure of the application is shown in Figure 2.
Investigators
investigator fill5,in
data
Pathogens 2016,
reply forms on a separate page (the so-called frontend). Inputted data are
10strictly and to guarantee optimal privacy. The structure of the GPIU study
stored securely in a specially-designed
application is designed to be adapted to MySQL database. Careclinical
other Internet-based has been takenin
studies tothe
separate
future.individual
investigator data strictly
investigator and toand
data strictly guarantee optimal
to guarantee privacy.
optimal The structure
privacy. of the GPIU
The structure of thestudy
GPIUapplication
study
application is designed to be adapted to other Internet-based clinical
is designed to be adapted to other Internet-based clinical studies in the future. studies in the future.

Figure 2. Structure of the Global Prevalence of Infections in Urology (GPIU) application on

FigureFigure 2. Structure
2. Structure of the of the Global
Global Prevalence
Prevalence of Infections
of Infections in Urology
in Urology (GPIU) application
(GPIU) application on
on the Internet.
the Internet.
the Internet.

The first
The page
page
The first
of
pageofthe
ofthe
website
thewebsite
(welcoming
(welcoming
website (welcoming
page)
page)
page)
presents
presents
presents
basic information
basic basic
aboutGPIU
information
information
the GPIU
about theabout
study
the GPIU
study
and and
study its
andaims (Figure 3). An investigator registers on this page. Subsequent
its aims (Figure 3). An investigator registers on this page. Subsequent to registration, the the
its aims (Figure 3). An investigator registers on this page. Subsequent to
to registration, the
investigator
investigator will
will gain
gain access
access to
to the
the web
web portal
portal of
of the
the study
study with
with aa username
username and
and
investigator will gain access to the web portal of the study with a username and personal password. personal
personal password.
Eachinvestigator/department
Each investigator/department
Each investigator/department is is isallocated
allocated
allocated aa centre
a centre number
centre number andpatient-unique
patient-unique
and patient-unique
number and study study
numbers
study numbers
through
numbers
the through
through
study the the
website. study
study The website.
website.
studyThe Thestudy
web study
portal web
web portal
portal
allows theallows
allows the
theinvestigator
investigator investigatorto navigate
to navigateto to datatoentry
navigate data entry
to data
and entry
help
and help functions from a single page, and he or she can fill in study forms, consult
functions from a single page, and he or she can fill in study forms, consult help pages and alter hisand
and help functions from a single page, and he or she can fill in study forms, help
consult pages
help and
pages or
alter
her alter
his or
personal hisher
or her personal
personal
information. information.
information.

Figure 3. Welcome page of the GPIU study.

The predefined workflow of the study is reflected on to the web-portal. The steps that are linked
with each other and occur in Figure
tandem3.asWelcome
follows: page
(i) registration
ofthe
theGPIU to the
GPIU study, (ii) input of hospital and
study.
Figure 3. Welcome page of study.
department information; and (iii) input of patient forms with infection (case report forms).
The predefined workflow of the study is reflected
5/8
on to the web-portal. The steps that are linked
with each other and occur in tandem as follows: (i) registration to the study, (ii) input of hospital and
department information; and (iii) input of patient forms with infection (case report forms).

5/8
Pathogens 2016, 5, 10 6 of 8

The predefined workflow of the study is reflected on to the web-portal. The steps that are
linked with each other and occur in tandem as follows: (i) registration to the study; (ii) input of
hospital and department information; and (iii) input of patient forms with infection (case report forms).
Investigators can fill in the patient forms, save the information and continue entries at another time.
A button for “validate” will appear only after all questions in the patient form are filled. Subsequent
to the user actively clicking on the “validate” button, the data will be submitted to the main patient
registry file.

3.4. Study Variables

Each participating department first completes the “Hospital Registration Form”, which details
the population of patients hospitalized in that department at 8:00 a.m. on the chosen study day.
Departments who previously participated will be provided with the “Hospital Registration Form” of
the previous year and are asked to update the information for each study year. An individual “Patient
Registration Form” is then completed for each patient categorized as having UTI or SSI (according to
CDC criteria [13]) and hospitalized in the participating urology department at 8:00 a.m. on the chosen
study day. Definitions of all requested variables included on the different forms are available by means
of help buttons.
Variable groups that are collected within the hospital and department forms are as follows:

‚ Geographical location
‚ Hospital size, setting, case volume
‚ Hospital and department infection control program
‚ Study day patient numbers (hospital and departmental)
‚ Urology department antibiotic practice program
‚ Study day antibiotic consumption

Variable groups that are collected within the patient forms are as follows:

‚ Demographics
‚ Comorbidities using the Charlson comorbidity score
‚ Interventions performed in the patient
‚ Antibiotics used
‚ Urine/surgical site/blood culture results
‚ Antimicrobial treatment for a current episode of infection (if given).

3.5. GPIU Side Studies

Apart from the GPIU main study, several side studies are/were taking place, dealing with
transurethral resection of the prostate (TURP), prostate biopsy, as well as urosepsis.

3.5.1. Prostate Biopsy Side Study

Since 2010, a side study designed to audit the prevalence of infective complications following
prostate biopsy has been carried out. Prostate biopsy is an extremely valuable and frequently
performed diagnostic procedure in urology. There is some evidence that infective complications
following prostate biopsy are increasing in number and severity in many countries possibly related to
increased resistance of faecal pathogens to antibiotics, such as fluoroquinolones used for prophylaxis.
The GPIU prostate biopsy side study is a prevalence study on infective complications of prostate
biopsy to audit the prevalence of infective complications after prostate biopsy across centres and
countries participating in the GPIU main study. Risk factors associated with a higher risk of infective
complications are evaluated, and changing resistance patterns to antibiotics used for prophylaxis are
determined. Furthermore, the prostate biopsy side study evaluates the antimicrobial management of
patients with post-biopsy infection and their clinical outcomes.
Pathogens 2016, 5, 10 7 of 8

Prostate Biopsy Study Design

All patients undergoing prostate biopsy during the 2-week period commencing on the GPIU study
day chosen by each centre should be included and followed up. Subsequent to registering patients
to the study, they are contacted 14 days following their biopsy and interviewed regarding infective
complications, either by telephone or face-to-face. The investigator for each centre will complete
a participant data file for each patient, including detailing relevant pre-biopsy characteristics, the
biopsy protocol followed and infective complications during the 14-day period following biopsy.

3.5.2. Transurethral Resection of the Prostate Side Study

From 2006 to 2009, a side study designed to audit the prevalence of infective complications
following transurethral resection of the prostate (TURP) was performed. The aim of this study was
to determine the prevalence of HAUTI and other complications of patients in the GPIU study that
received a TURP. Interventional and patients’ specific risk factors were evaluated.

3.5.3. Urosepsis Side Study (Serpens Study)

Comparing the different HAUTIs between 2003/2004 and 2008 showed that severe infections,
such as pyelonephritis and urosepsis, were more prevalent in 2008 compared to 2003/2004. A further
investigation of the subcohort of patients with urosepsis from 2003 to 2013 corroborated this finding
and led to the design of a prospective study on urological patients with urosepsis, which is currently
being conducted.

3.6. Microbiological Investigations

All urine cultures and other microbiological investigations are conducted in the local laboratories
according to their microbiological standards. Information about the standard used for antimicrobial
susceptibility testing is provided by most of the centres.

3.7. Statistical Analysis of Data

Study data were imported from the web-based survey into Microsoft Access (Microsoft Corp,
Seattle, WA, USA), as a comma separated file (csf), and reorganized. The data files were transferred to
statistical packages for analysis.
The initial review of each year’s data is carried out descriptively. Followed by this, pooled analysis
of data is carried out in a similar manner to identify any emerging trends. Finally, the pooled data are
further carried into statistical modelling to explain any trends that may have been identified.
In the case of antimicrobial susceptibility changes over the years, resistance rates are specified by
bacterial species and antibiotics tested for each consecutive year. Geographic differences were assessed
according to 4 regions (North Europe, South Europe, Asia, Africa + South America (for statistical
reasons due to low case numbers, Africa and America were merged)). South European countries
were defined as European countries with a shore on the Mediterranean Sea and North Europe as the
remaining European countries.

4. Conclusions
The GPIU study is an annual, worldwide-conducted prevalence study to survey infections in
urological patients on an annual basis since 2003. Antibiotic resistance rates are very high in all
locations, and antibiotic usage is not always optimal. Therefore, this study can help to deliver data
for guideline recommendations of adequate empirical antibiotic therapy in hospitalized urological
patients. Knowledge of regional and local resistance data and prudent use of antibiotics, however,
continue to be important strategies to optimize antibiotic therapy in urological patients with infections.

Acknowledgments: This study was organized by the board of the ESIU, endorsed and sponsored by the
EAU and performed in collaboration with the Asian Association of UTI and STD, the International Society
Pathogens 2016, 5, 10 8 of 8

of Chemotherapy for Infection and Cancer and the Interregional Association of Clinical Microbiology and
Antimicrobial Chemotherapy, as well as numerous regional urological and infectious diseases societies. The GPIU
study group is most grateful to the altruistic contributions of the GPIU investigators.
Author Contributions: Data acquisition: Florian Wagenlehner, Zafer Tandogdu, Riccardo Bartoletti,
Tommaso Cai, Mete Cek, Ekaterina Kulchavenya, Bela Koves, Kurt Naber, Tamara Perepanova, Peter Tenke,
Bjorn Wullt, Florian Bogenhard, Truls Erik Bjerklund Johansen. Data evaluation: Florian Wagenlehner,
Zafer Tandogdu, Florian Bogenhard, Truls Erik Bjerklund Johansen.
Conflicts of Interest: The authors declare no conflict of interest.

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