J Antimicrob Chemother 2016; 71: 1106 – 1117

doi:10.1093/jac/dkv418 Advance Access publication 8 January 2016

The Worldwide Antibiotic Resistance and Prescribing in European

Children (ARPEC) point prevalence survey: developing hospital-quality
indicators of antibiotic prescribing for children
Ann Versporten1, Julia Bielicki2, Nico Drapier1, Mike Sharland2 and Herman Goossens1*
on behalf of the ARPEC project group†

1
Laboratory of Medical Microbiology, Vaccine & Infectious Disease Institute (VAXINFECTIO), Faculty of Medicine and Health Science,
University of Antwerp, Antwerp, Belgium; 2Paediatric Infectious Diseases Research Group, Institute for Infection and Immunity,
St George’s, University of London, London, UK

*Corresponding author. Tel: +32-38213789; Fax: +32-32652663; E-mail: herman.goossens@uza.be

†Members are listed in the Acknowledgements section.

Received 24 August 2015; returned 19 September 2015; revised 28 October 2015; accepted 5 November 2015

Objectives: Previously, web-based tools for cross-sectional antimicrobial point prevalence surveys (PPSs) have
been used in adults to develop indicators of quality improvement. We aimed to determine the feasibility of devel-
oping similar quality indicators of improved antimicrobial prescribing focusing specifically on hospitalized
neonates and children worldwide.
Methods: A standardized antimicrobial PPS method was employed. Included were all inpatient children and neo-
nates receiving an antimicrobial at 8:00 am on the day of the PPS. Denominators included the total number of
inpatients. A web-based application was used for data entry, validation and reporting. We analysed 2012 data
from 226 hospitals (H) in 41 countries (C) from Europe (174H; 24C), Africa (6H; 4C), Asia (25H; 8C), Australia (6H),
Latin America (11H; 3C) and North America (4H).
Results: Of 17 693 admissions, 6499 (36.7%) inpatients received at least one antimicrobial, but this varied con-
siderably between wards and regions. Potential indicators included very high broad-spectrum antibiotic prescrib-
ing in children of mainly ceftriaxone (ranked first in Eastern Europe, 31.3%; Asia, 13.0%; Southern Europe, 9.8%),
cefepime (ranked third in North America, 7.8%) and meropenem (ranked first in Latin America, 13.1%). The sur-
vey identified worryingly high use of critically important antibiotics for hospital-acquired infections in neonates
(34.9%; range from 14.2% in Africa to 68.0% in Latin America) compared with children (28.3%; range from 14.5%
in Africa to 48.9% in Latin America). Parenteral administration was very common among children in Asia (88%),
Latin America (81%) and Europe (67%). Documentation of the reasons for antibiotic prescribing was lowest in
Latin America (52%). Prolonged surgical prophylaxis rates ranged from 78% (Europe) to 84% (Latin America).
Conclusions: Simple web-based PPS tools provide a feasible method to identify areas for improvement of antibiotic
use, to set benchmarks and to monitor future interventions in hospitalized neonates and children. To our knowledge,
this study has derived the first global quality indicators for antibiotic use in hospitalized neonates and children.

role of antibiotic stewardship.3 Also, President Obama of the USA

Introduction
Antimicrobial resistance is a major public health problem and con-
tinuing progress in the treatment of many infections is threatened
by the growing resistance of pathogens to antimicrobial agents.1
Judicious use of antibiotics is essential to slow the emergence of
antibiotic resistance in bacteria and extend the useful lifetime of
effective antibiotics.2 The 2011 European Commission Action Plan
against the rising threats from antimicrobial resistance empha-
sized the importance of surveillance data with regard to anti-
microbial use and resistance at local and national levels and the
has recently increased efforts to combat and prevent antibiotic
resistance, among which is the core aim of improving the quality
of antibiotic prescribing.4,5
Access to standardized and validated antibiotic surveillance
data is essential to assess the appropriateness of antimicrobial
prescriptions and to set and monitor outcomes of interventions.
There is as yet no consensus regarding the use of indicators to
monitor trends of antibiotic use in hospitals.6 The European
Surveillance of Antimicrobial Consumption (ESAC) project devel-
oped and validated a web-based point prevalence survey (PPS)

# The Author 2016. Published by Oxford University Press on behalf of the British Society for Antimicrobial Chemotherapy. All rights reserved.
For Permissions, please e-mail: journals.permissions@oup.com

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 Global Point Prevalence Survey in hospitalized children in 2012
tool to evaluate hospital antimicrobial prescribing rates at local
and national level. The ESAC-PPS identified inappropriate use
linked to specific agents or specialties, proposed quality indicators
of prescribing practices and identified targets to improve anti-
microbial prescribing.7 – 9 The ESAC-PPS tool was used to set quan-
titative targets for improved antibiotic prescribing in adults and to
measure the effectiveness of interventions to reach these targets
through repeated PPSs.10,11
Currently, no comparable detailed information on antibiotic use
in hospitalized neonates and children is available. Longitudinal sur-
veys of antimicrobial use in neonates and children are in part lack-
ing because there is no consensus on the indicators that should be
used to monitor trends of antibiotic use. PPS tools were not specif-
ically designed for capturing antimicrobial prescribing data in this
population. As part of the Antibiotic Resistance and Prescribing in
European Children (ARPEC) project,12 the ESAC-PPS tool was specif-
ically adapted to survey antimicrobial use in hospitalized neonates
and children (ARPEC-PPS; work package 5). The feasibility of carry-
ing out the ARPEC-PPS method in a large number of hospitals was
piloted in 73 hospitals from 23 different countries in 2011.13 After a
successful pilot study, this survey was subsequently rolled out as a
global ARPEC-PPS in a very large set of hospitalized neonates and
children worldwide.
The study aimed to describe antibiotic prescribing practices
among hospitalized neonates and children worldwide and to
determine the feasibility of adapting existing adult quality indica-
tors of optimal prescribing to neonates and children.
Materials and methods
Ethics
This study was a completely anonymized audit of current antimicrobial
prescribing practices. No unique identifiers were entered into the data-
base. Every patient record was given a unique non-identifiable survey
number, which was automatically generated by a computer program spe-
cifically designed for anonymous data entry. Formal ethics approval for
this study depended on the country and was taken care of by each partici-
pating hospital if required.
Countries and hospitals
Paediatric infectious disease specialists, clinical microbiologists and pharma-
cists, and other interested healthcare professionals from established net-
works such as the European Society of Paediatric Infectious Diseases14 and
Global Research in Paediatrics,15 were invited to participate in this worldwide
ARPEC-PPS conducted in October–November 2012. We collected data from
226 hospitals from 41 countries belonging to the six United Nations (UN)
regions (Africa, Asia, Oceania, Latin America, North America and Europe).16
For Europe, four geographical UN sub-regions were defined:16 Eastern
Europe (Hungary, 1 hospital; Poland, 1 hospital; Romania, 2 hospitals),
Northern Europe (Denmark, 4; Estonia, 2; Finland, 1; Latvia, 10; Lithuania, 1;
UK, 65), Southern Europe {Croatia, 2; Greece, 5; Italy, 7; Kosovo [in accordance
with UN Security Council resolution 1244 (1999)], 3; Former Yugoslav Republic
of Macedonia, 1; Malta, 1; Portugal, 3; Slovenia, 4; Spain, 13}, Western Europe
(Belgium, 14; France, 9; Germany, 22; Luxembourg, 1; the Netherlands, 1;
Switzerland, 1). Hospital numbers for other regions were as follows: Africa
(Gambia, 2; Ghana, 2; Malawi, 1; South Africa, 1); Asia (Bahrain, 1; Georgia, 6;
India, 8; Iran, 3; Kuwait, 3; Oman, 1; Saudi Arabia, 2; Singapore, 1); Oceania
(Australia, 6); Latin America (Argentina, 1; Colombia, 6; Mexico, 4); and
North America (USA, 4).
Hospitals were classified as (i) primary, (ii) secondary and (iii) tertiary,
specialized care and infectious diseases hospitals.17
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JAC
Four main paediatric ward types were defined: general paediatric med-
ical wards (GPMWs); paediatric surgical wards (PSWs); paediatric intensive
care units (PICUs); and specialized paediatric medical wards (SPMWs). The
last type included haematology/oncology special paediatric medical
wards (HO-SPMWs), cardiology wards (C-SPMWs), transplant wards
(bone marrow transplant/solid) (T-SPMWs) and all others (other-SPMWs).
Neonatal wards included three aggregated neonatal intensive care unit
(NICU) levels providing special care (NICU level 1), high-dependency care
to low birth weight neonates (NICU level 2) or tertiary referral care to very
low birth weight neonates (NICU level 3), and a general neonatal medical
ward (GNMW).18
Data collection
As described in full detail elsewhere,13 participants were asked to conduct
a 1 day cross-sectional PPS during which all paediatric and neonatal wards
had to be audited once within a fixed period of time. The PPS included all
neonates (,30 days) and children ,18 years old present in the ward at
8:00 am at least since midnight on the day of the survey. Data collection
was based on the standardized ESAC-PPS protocol. For each patient receiv-
ing at least one antimicrobial, mandatory data included prescribed anti-
microbial agent (dose per administration, number of doses per day and
route of administration), age and gender, indication for treatment
(community-acquired, hospital-acquired, surgical prophylaxis and medical
prophylaxis), reason for treatment according to a predefined list, speciality
(medicine, surgery or intensive care) and whether the reasons for treat-
ment were documented in the patient notes. Information on surgical
prophylaxis was captured for the previous 24 h, indicating 1 dose, 1 day
or .1 day. The ESAC-PPS protocol was further adapted for the purpose
of collecting data on children and neonates. Additional mandatory vari-
ables included: underlying diagnosis according to predefined lists of com-
mon medical and surgical conditions in children and neonates; whether
the treatment was targeted (based upon microbiological culture and sen-
sitivity testing) or empirical; and current weight and ventilation status. For
premature neonates, birth weight and gestational age were also collected.
Denominators included the total number of patients present on the ward
at 8:00 am and the total number of beds by the predefined six different
paediatric and four neonatal department types.
Drugs were classified according to the standardized and internationally
recognized WHO Anatomical Therapeutic Chemical (ATC) classification
system classifying drugs according to their main therapeutic use. 19
Antibiotics were grouped into antibacterials for systemic use (ATC J01),
oral metronidazole (ATC P01AB01), intestinal anti-infectives (oral antibio-
tics vancomycin, paromomycin and colistin, ATC A07AA) and antibiotic
drugs for the treatment of tuberculosis (rifampicin, ATC J04AB02).
Antimycotics for systemic use (ATC J02) were merged with antifungals
classified under the intestinal anti-infectives (ATC A07AA: oral nystatin,
amphotericin B, miconazole). We further collected data on antivirals for
systemic use (ATC J05), nitroimidazole derivatives (ATC P01AB) and anti-
malarials (ATC P01B).
Data collection was performed using paper forms, after which data
were entered into a central database using a web-based application for
data entry, validation and reporting. All data were mandatorily entered
online. The software was designed to avoid missing data (e.g. it was not
possible to enter incomplete patient and denominator files online and
complete the submission). The data validation procedure involved extra
checks on erroneous data entry, e.g. extremely high antibiotic prevalence
rates, possibly involving wrong denominators, and extremely high dosing.
All data were completely anonymously entered into the database and
safeguarded at the University of Antwerp, Belgium. A helpdesk as well
as a frequently asked question list were available in support of the partici-
pants. Participation was exclusively on a voluntary basis and the numbers
of hospitals and patients were not intended to be representative of a coun-
try or region. Depending on the countries’ legal requirements, hospitals
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had to comply with local ethics approval. A data privacy excerpt document
was made available for this purpose. Informed consent was not needed
because the survey did not require direct involvement or contact with
the patient, treatment or other intervention.
Data analysis
For this paper, antimicrobial use is reported as the number of treated
patients and the number of therapies. Therapy was defined as the use
of one substance in one route of administration. Antimicrobial prescrib-
ing rates and the derived potential quality indicators (Table 1) are
expressed as percentages (proportional use), means and/or ranges
aggregated at UN regional level,16 by ward type, by indication (thera-
peutic or prophylactic antibiotic prescribing) or according to age category
(children aged .1 month and neonates aged ,30 days). We also ranked
the number of antibacterials for systemic use (ATC code J01) accounting
for 90% and 75% of (antibiotic) drug utilization (DU90% and DU75%,
respectively).
Results
General overview
The 2012 ARPEC-PPS was performed in 226 hospitals from 41 coun-
tries and included 22 primary (515 patients, 3%), 81 secondary
(3074 patients, 17%) and 123 tertiary (14 104 patients, 80%)
care hospitals. Data on admissions to 1482 wards (17693 patients)
were recorded, and included 444 GPMWs (5298 patients), 327
SPMWs (3584 patients), 240 NICUs (3515 patients), 201 PSWs
(2273 patients), 135 PICUs (1062 patients) and 135 GNMWs
(1961 patients). Overall, 56% of treated children were males
(range, from 49% in Africa to 59% in Latin America). Among anti-
microbial prescriptions for children, antibiotics represented 85.7%
(n¼7987), followed by antimycotics (9.6%, n¼891) and antivirals
(4.7%, n¼ 446). Among antimicrobial prescriptions for neonates,
antibiotics represented 89.2% (n¼2298), followed by antimycotics
(8.8%, n¼227) and antivirals (1.9%, n¼50).

Table 1. Overview of the suggested antibiotic quality indicators

Potential indicators of antibiotic prescribing
Potential antimicrobial quality indicators for hospitalized neonates Table 2 provides antibiotic prevalence rates and selected quality
and children indicators by ward type. Out of 17 693 patients, 6499 (36.7%)
received at least one antimicrobial, with the highest rates
1. Documentation of the reason for antimicrobial prescribing in the observed among PICUs (61.3%) and SPMWs (46.0%). Overall
notesa baseline recording of the reason for antibiotic therapy or prophy-
2. Targeted therapeutic antibiotic prescribinga laxis was 73.3% (range, from 81.7% in Africa to 53.3% in Latin
3. Parenteral administration of antibioticsa America). Overall proportional targeted therapeutic antibiotic pre-
4. Number of antibiotic combination therapiesa scribing was 22.3% (Latin America, 28.9%; North America, 27.9%;
5. Broad-spectrum antibiotic prescribingb Asia and Australia, 27.8%; Africa, 21.8%; Europe, 19.5%). At least
6. Antibiotic prevalence rates for hospital-acquired infectionsc one parenteral antibiotic was recorded in 78.6%, with substantial
7. Targeted broad-spectrum antibiotic prescribing for hospital-acquired regional variation among children aged .1 month (Asia, 88.2%;
infectionsc Latin America, 81.2%; Africa, Europe and Australia, 68.7%;
8. Empirical broad-spectrum antibiotic prescribing for North America, 57.5%), while being higher for neonates (up to
community-acquired infectionsc 98.2%). In total, 322 different antibiotic combinations at ATC4
9. Broad-spectrum antibiotic prescribing for surgical prophylaxisd level (chemical subgroup; see e.g. Figure 1 for a subset of the clas-
10. Prolonged antibiotic prescribing for surgical prophylaxisd sification categories) were recorded worldwide.

a
See Table 2.
b
See Figures 1 and 2 and Tables 3 and 4.
Antibiotic drug utilization at regional level in children
c
See the Results section ‘Therapeutic prescribing’ and Tables 6 and 7. Figure 1 reports the most commonly prescribed antibiotics among
d
See the Results section, last paragraph. children. In all regions except North America, b-lactams made up

Table 2. Overview of antibiotic prevalence rates and quality indicators by ward type

Patients Targeted Parenteral Antibiotic

Patients treated Prescriptions Reason in treatment administration combination
Ward type (n) [n (%)] (n) notes (%) (%) (% of patients) (% of patients)

Paediatric intensive care unit (PICU) 1062 651 (61.3) 1113 74.1 25.7 89.7 50.7
Specialized paediatric medical ward (SPMW) 3584 1648 (46.0) 2662 67.9 27.4 66.1 40.7
General paediatric medical ward (GPMW) 5298 2091 (39.5) 2929 76.4 19.7 74.3 31.6
Paediatric surgical ward (PSW) 2273 803 (35.3) 1135 63.3 19.0 78.1 32.6
Neonatal intensive care unit (NICU) 3515 1065 (30.3) 1933 82.7 18.7 95.6 71.2
General neonatal medical ward (GNMW) 1961 241 (12.3) 424 68.2 27.9 96.7 70.1

Total 17693 6499 (36.7) 10196 73.3 22.3 78.6 43.8

All indicators were calculated at patient level, with the exception of Reason in notes and Targeted treatment, which were calculated at prescription level.
For targeted treatment, selection has been made for therapeutic antibiotic use only (HAI and CAI).
Gambia, with outlying results for targeted use, was removed from analyses.

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 Global Point Prevalence Survey in hospitalized children in 2012 JAC
100%
Other antibacterials
90%
Glycopeptides (J01XA)
80% Comb. sulphonamides and trimethoprim (J01EE)
70% Aminoglycosides (J01GB)

60% Carbapenems (J01DH)

50% 4th-gen. Cephalosporins (J01DE)

40% 3rd-gen. Cephalosporins (J01DD)

2nd-gen. Cephalosporins (J01DC)

30%
1st-gen. Cephalosporins (J01DB)
20%
Comb. of penicillins with b-lactam. inh. (J01CR)
10%
Penicillins with extended spectrum (J01CA)
0%
b-lactam. Resist. Penicillins (J01CF)
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Figure 1. Proportion of prescribed antibiotics (ATC4 level) among children (.1 month) by region. The pale grey part of the stacked bars represents other
antibacterial subgroups. This figure appears in colour in the online version of JAC and in black and white in the print version of JAC.

more than half of all antibiotic prescriptions. Third-generation
cephalosporins were most frequently prescribed in Eastern
Europe (35.7%) and Asia (28.6%), fourth-generation cephalospor-
ins (cefepime) in North America (7.8%) and carbapenems in Latin
America (13.3%). A considerable amount of narrow-spectrum
antibiotics was prescribed in Africa and Northern Europe (e.g.
b-lactamase-sensitive penicillins, 11.0% and 4.3%, respectively)
and Australia (e.g. first-generation cephalosporins, 9.6%).
Table 3 reports the specific antibiotics prescribed to children by
UN region, ranked at overall DU90%. In total, 77 different systemic
antibiotic substances (ATC J01) were administered to children.
Ceftriaxone (8.5% of total use of antibiotics) ranked first in
Eastern Europe, Asia and Southern Europe (31.3%, 13.0% and
9.8%, respectively). In Western Europe and Australia, cefotaxime
was more popular than ceftriaxone (4.8% and 5.6%, respectively),
while cefepime was more commonly prescribed in North America
(7.8%). The second most prescribed antibiotic was sulfamethoxa-
zole/trimethoprim (7.2% of total antibiotic use), ranking first in
Western Europe (11.4%), North America (11.2%) and Australia
(10.0%). Vancomycin ranked second in Latin America (12.9%),
North America (10.6%) and Asia (8.5%). Meropenem ranked first
in Latin America (13.1%).
Antibiotic drug utilization at regional level in neonates
Figure 2 shows the most prevalently prescribed antibiotics among
neonates. Aminoglycosides in combination with either ampicillin/
amoxicillin (Western and Southern Europe, Asia, Latin America
and North America) or benzylpenicillin (Northern Europe, Africa
and Australia) were by far the most frequently used regimens.
Table 4 shows the antibiotics prescribed to neonates by
UN region, ranked at overall DU90%. In total, 43 different systemic
antibiotic substances were prescribed to neonates worldwide.
Gentamicin (23.6% of total antibiotic use) ranked first in
Africa (36.3%), Australia (32.8%), North America (31.3%) and
Northern Europe (29.1%). The second most prescribed antibiotic
was ampicillin (15.3% of total antibiotic use), ranking first in
Southern Europe (29.5%), Latin America (29.0%), Asia (24.3%)
and Western Europe (18.4%). The third most popular antibiotic
was benzylpenicillin (12.8% of total antibiotic use), ranking
second in Northern Europe (28.2%), Australia (24.6%) and Africa
(21.6%), while absent in the DU90% of Southern and Western
Europe, Latin America and North America. Aminoglycosides
were most often prescribed in combination with ampicillin or
benzylpenicillin.
Antibiotic prescribing by indication
The most frequently recorded reason to treat children was a bac-
terial lower respiratory tract infection (18.7%) and that to treat
neonates was sepsis (36.4%) (see Table 5 for the top 10 reasons
for antibiotic treatment in children and neonates).
Tables 6 and 7 compare therapeutic (community-acquired ver-
sus hospital-acquired; empirical versus targeted treatment) and
prophylactic prescribing in children and neonates: 75.3% of anti-
biotics were prescribed therapeutically (75.4% in children and
74.9% in neonates) and 24.7% prophylactically (14.8% for med-
ical and 9.8% for surgical prophylaxis in children and 19.5% for
medical and 5.6% for surgical prophylaxis in neonates).
Therapeutic prescribing Overall, hospital-acquired infections
(HAIs) accounted for 49.9%, 34.9%, 33.7%, 28.9%, 28.5% and
14.4% of all therapeutic antibiotic prescriptions in Latin America,
Asia, North America, Europe, Australia and Africa, respectively. Of
all antibiotics administered for an HAI, 29.9% were recorded as
being targeted based on microbiological results (range, from
23.8% in Africa to 39.4% in Australia). Overall, antibiotics were
more commonly prescribed for HAIs in neonates (34.9%; range,
from 14.2% in Africa to 68.0% in Latin America) compared with

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Versporten et al.
Table 3. Most prescribed antibiotics (ATC J01; 5th level) to children (≥30 days old) (%) by UN regiona, ranked at overall drug utilization 90% (DU90%)

Northern Southern
Eastern Europe (n¼112) Europe (n¼1806) Europe (n¼1558) Western Europe (n¼1157) Africa (n¼ 491) Asia (n¼ 1094) Australia (n¼502) Latin America (n¼528) North America (n¼463)

ceftriaxone 31.3 amoxicillin/inhib. 13.6 ceftriaxone 9.8 sulfa./trimethoprim 11.4 gentamicin 16.3 ceftriaxone 13.0 sulfa./ 10.0 meropenem 13.1 sulfa./trimethoprim 11.2
trimethoprim
ampicillin 10.7 amoxicillin 7.1 amoxicillin/inhib. 7.6 amoxicillin/inhib. 8.1 ceftriaxone 14.1 vancomycin 8.5 piperacillin/inhib. 7.6 vancomycin 12.9 vancomycin 10.6
sulfa./trimethoprim 8.0 ceftriaxone 6.9 sulfa./ 7.4 cefuroxime 6.7 benzylpenicillin 10.2 cefotaxime 8.2 gentamicin 7.6 ceftriaxone 11.6 cefepime 7.8
trimethoprim
cefuroxime 5.4 cefuroxime 5.5 piperacillin/inhib. 5.5 amoxicillin 5.6 cefuroxime 9.8 amikacin 7.4 cefazolin 7.6 clindamycin 7.6 azithromycin 7.6
ampicillin/inhib. 4.5 sulfa./ 5.3 meropenem 4.7 vancomycin 4.8 sulfa./ 8.1 meropenem 7.1 amoxicillin 6.2 amikacin 6.6 clindamycin 6.5
trimethoprim trimethoprim
procaine 4.5 flucloxacillin 5.3 gentamicin 4.6 cefotaxime 4.8 ampicillin 5.1 piperacillin/inhib. 5.4 flucloxacillin 6.2 piperacillin/inhib. 5.1 cefazolin 6.5
benzylpenicillin
amikacin 3.6 gentamicin 5.1 teicoplanin 4.6 meropenem 4.6 cloxacillin 4.1 ceftazidime 4.5 ticarcillin 6.0 cefalotin 4.7 piperacillin/inhib. 5.8
azithromycin 3.6 azithromycin 4.5 metronidazole 4.5 piperacillin/inhib. 4.5 chloramphenicol 3.5 cefuroxime 4.2 cefotaxime 5.6 ciprofloxacin 3.2 amoxicillin 5.0
levofloxacin 3.6 cefotaxime 4.4 cefotaxime 4.3 gentamicin 4.2 amoxicillin/inhib. 3.3 metronidazole 4.2 vancomycin 5.2 sulfa./ 3.0 ceftriaxone 4.3
trimethoprim
vancomycin 2.7 piperacillin/inhib. 4.0 ceftazidime 4.0 colistin 3.8 ciprofloxacin 3.3 sulfa./ 3.7 amoxicillin/inhib. 3.8 ampicillin 3.0 gentamicin 3.5
trimethoprim
piperacillin/inhib. 2.7 clarithromycin 3.9 amikacin 3.9 metronidazole 3.5 metronidazole 2.9 ampicillin/inhib. 3.1 metronidazole 3.8 trimethoprim 3.0 ampicillin 3.5
gentamicin 2.7 metronidazole 3.7 ampicillin 3.9 ampicillin 3.0 meropenem 2.4 clindamycin 2.9 azithromycin 3.8 amoxicillin 2.8 tobramycin 3.5
cefoperazone 2.7 meropenem 3.5 cefuroxime 3.6 teicoplanin 2.9 amikacin 2.4 clarithromycin 2.7 ceftriaxone 3.2 metronidazole 2.7 metronidazole 2.4
comb.
nalidixic acid 2.7 benzylpenicillin 3.0 vancomycin 3.5 ceftriaxone 2.9 flucloxacillin 2.4 amoxicillin/inhib. 2.7 tobramycin 2.8 ampicillin/inhib. 2.7 ciprofloxacin 2.4
meropenem 1.8 vancomycin 2.4 ciprofloxacin 2.8 ceftazidime 2.8 amoxicillin 1.8 cefazolin 2.3 ciprofloxacin 2.6 cloxacillin 2.7 cefalexin 2.4
ceftazidime 2.4 clarithromycin 2.5 cefazolin 2.2 ampicillin 2.2 benzylpenicillin 2.2 cefotaxime 2.1 trimethoprim 2.2
ciprofloxacin 2.1 clindamycin 2.3 amikacin 2.1 cefoperazone. 2.0 cefalexin 2.0 clarithromycin 1.9 phenoxymethylpenicillin 1.9
comb.
tobramycin 1.9 amoxicillin 2.1 ciprofloxacin 2.1 gentamicin 1.6 meropenem 1.6 cefepime 1.7 erythromycin 1.9
cefazolin 1.7 ampicillin/inhib. 1.9 tobramycin 1.9 ciprofloxacin 1.5 lincomycin 1.6 meropenem 1.7
clindamycin 1.7 trimethoprim 1.7 imipenem/inhib. 1.9 cloxacillin 1.5 amikacin 1.4
teicoplanin 1.6 ceforanide 1.5 trimethoprim 1.6 azithromycin 1.2
cefazolin 1.4 phenoxymethylpenicillin 1.5
azithromycin 1.3 clindamycin 1.4
cefepime 0.9 azithromycin 1.1
ampicillin/inhib. 1.1

sulfa., sulfamethoxazole; inhib., b-lactamase inhibitor; comb., combination.

Grey shading indicates drug utilization 75% (DU75%) by UN region.
a
Number of countries included from each region: Eastern Europe (3), Northern Europe (6), Southern Europe (9), Western Europe (6), Africa (4), Asia (8), Australia (1), Latin America (3), North
America (1).

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 Global Point Prevalence Survey in hospitalized children in 2012 JAC
100%
Other antibacterials
90% Glycopeptides (J01XA)
80% Imidazole derivatives (J01XD)
70% Aminoglycosides (J01GB)
60% Carbapenems (J01DH)
50% 4th-gen. Cephalosporins (J01DE)

40% 3rd-gen. Cephalosporins (J01DD)

30% 2nd-gen. Cephalosporins (J01DC)

20% 1st-gen. Cephalosporins (J01DB)

10% Comb. of penicillins with b-lactam. inh. (J01CR)

0% Penicillins with extended spectrum (J01CA)

b-lactam. Resist. Penicillins (J01CF)

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Figure 2. Proportion of prescribed antibiotics (ATC4 level) among neonates (,30 days) by region. The pale grey part of the stacked bars represents other
antibacterial subgroups. There are no data for Eastern Europe. This figure appears in colour in the online version of JAC and in black and white in the print
version of JAC.

children (28.3%; range, from 14.5% in Africa to 48.9% in Latin
America). Glycopeptides (mainly vancomycin) were most often pre-
scribed for HAIs in Latin America, North America, Australia and
Europe (26.2%, 21.7%, 17.3% and 20.4% of total antibiotic use
for HAIs, respectively), followed by carbapenems (mainly merope-
nem) in Latin America, Africa, Asia and Europe (24.0%, 21.9%,
16.1% and 13.3%, respectively). Use of cefepime for HAIs was
15.7% in North America, but ,2% elsewhere.
Of all antibiotics administered for community-acquired infec-
tions (CAIs), 19.1% were targeted (range, from 16.0% in Europe
to 27.9% in North America). The most commonly prescribed
antibiotics for CAIs were third-generation cephalosporins (mainly
ceftriaxone) in Asia, Latin America and Europe (32.8%, 23.5%
and 18.7% of total antibiotic use for treatment of CAIs, respect-
ively) followed by aminoglycosides (mainly gentamicin) in Africa,
Australia and Europe (26.6%, 17.6% and 14.6%, respectively),
broad-spectrum penicillins (mainly amoxicillin) in North America,
Europe and Australia (14.5%), combinations of penicillins with an
enzyme inhibitor (mainly co-amoxiclav) in Europe, North America
and Australia (14.2%, 11.9% and 10.0%, respectively), narrow-
spectrum penicillins (mainly benzylpenicillin) in Africa (16.5%),
and clindamycin in Latin and North America (12.0% and 10.2%,
respectively).
Prophylactic prescribing Medical prophylactic prescribing
accounted for 64.3% of all prophylactic antibiotic prescribing, ran-
ging from 55.8% in Asia to 82.9% in Africa. Overall, antibiotics
were more commonly prescribed for medical prophylaxis in neo-
nates (77.8%; range, from 28.6% in Africa to 89.1% in Australia)
compared with children (60.3%; range, from 42.9% in Asia to
96.4% in Africa) (Tables 6 and 7). Many different antibiotics were
prescribed for medical prophylactic use, with sulfamethoxazole/
trimethoprim dominating in Africa, North America, Australia
and Europe (79.3%, 36.2%, 34.2% and 30.5% of total medical
prophylactic prescribing, respectively) and ampicillin in Latin
America and Asia (21.5% and 15.9%, respectively).
Surgical prophylactic prescribing accounted for 39.7% of all
prophylactic antibiotic prescribing in children, compared with
22.2% in neonates (Tables 6 and 7). Most antibiotics for surgical
prophylactic use were first-generation cephalosporins, mainly
cefazolin in North America and Australia (61.1% and 47.0% of
total surgical prophylactic prescribing, respectively) and cefalotin
in Latin America (27.5%), followed by third-generation cephalos-
porins (mainly ceftriaxone) in Asia and Europe (25.6% and 14.6%,
respectively), second-generation cephalosporins (mainly cefurox-
ime) (17.5%) or combinations of penicillins with enzyme inhibitors
(mainly co-amoxiclav) in Europe (16.6%). Prolonged surgical
prophylaxis (.1 day) was very common in all regions, ranging
from 78% in Europe to 84% in Latin America.
Discussion
This global ARPEC-PPS for the first known time explored the feasi-
bility of producing qualitative indicators to uniformly assess anti-
microbial prescribing, to identify key areas of poor practice and to
propose benchmarks for improved antibiotic prescribing among
hospitalized neonates and children worldwide.
Overall, we found less regional difference in antibiotic prescrib-
ing among hospitalized neonates than among children. The dom-
inance of gentamicin used in combination with benzylpenicillin or
ampicillin across all regions was very striking, and explains the
high proportion of antibiotics used in combination among neo-
nates (around 70%). Remarkably high use of amikacin was
noted in neonates admitted to Western European, Southern
European, Asian and Latin American hospitals, and, worryingly,
meropenem was widely prescribed to Asian neonates.
In contrast, we observed striking regional differences in anti-
biotic prescribing among hospitalized children. A high proportion

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 Versporten et al.

of African, Australian, Western European and Northern European

8.3
6.3
gentamicin 31.3

clindamycin 4.2
29.2
amoxicillin 10.4

Number of countries included from each region: Northern Europe (6), Southern Europe (9), Western Europe (6), Africa (4), Asia (8), Australia (1), Latin America (3), North America (1).
America (n ¼48)

children continued to receive older narrow-spectrum antibiotics,

mainly benzylpenicillin, sulfamethoxazole/trimethoprim, amoxi-
North

cefotaxime
ampicillin
cillin and gentamicin. Africa was characterized by considerably
cefazolin high use of gentamicin, often in combination with benzylpenicillin.
Eastern European, Southern European, Asian, North American and
Latin American children received considerably more broad-
8.7
29.0
14.5

11.6

2.9
4.3

4.3
2.9
13.0
Latin America (n ¼69)

spectrum antibiotics, mainly third-generation cephalosporins,

cefepime and meropenem.
The prevalence of broad-spectrum agent use is an important
meropenem

quality indicator in children. The high use seen here may be par-
12.3 vancomycin

3.3 piperacillin/
benzylpenicillin 24.6 gentamicin

8.2 cefotaxime

penicillin
Table 4. Most prescribed antibiotics (ATC J01; 5th level) to neonates (,30 days old) (%) by UN regiona, ranked at overall drug utilization 90% (DU90%)

cloxacillin
32.8 ampicillin

tially explained by the remarkably high antibiotic prescribing rates

9.0 amikacin

procaine
inhib.

for HAIs as an indication, e.g. in Latin America (49.9%), Asia

(34.9%) and North America (33.7%), again with high proportions
of meropenem, ceftriaxone and cefepime use. The striking finding
Australia (n¼122)

of the high number of antibiotics prescribed for HAIs in neonates,

reaching 68% of all therapeutic prescribing in Latin America,
requires further investigation. In Europe we observed slightly
flucloxacillin
vancomycin
gentamicin

cefotaxime
amoxicillin

lower prevalence rates of antimicrobials prescribed for an HAI

(28.9%), comparable to the ESAC 2009-PPS (adults and children,
30.7%)8 and the ECDC 2010-PPS (paediatric wards, 30.3%).20
High proportions of broad-spectrum antibiotic use could be
explained by regionally high rates of ESBL-producing or carbapenem-
13.9
24.3

11.8
9.9
8.7

2.4
2.9
7.0

6.7

1.9
1.4

resistant Gram-negative organisms. Surveillance programmes in

Asia (n¼416)

Latin America in adults and children have demonstrated an increas-

benzylpenicillin
metronidazole

ing trend of resistance to extended-spectrum cephalosporins with

4.9 meropenem

3.7 vancomycin

ceftazidime
4.1 piperacillin/
benzylpenicillin 21.6 gentamicin

5.7 cefotaxime

high prevalence of ESBL-producing Escherichia coli and Klebsiella

cloxacillin
36.3 ampicillin

13.5 amikacin

inhib.

spp. and carbapenem-resistant Klebsiella spp.21,22 Similarly, in Asia

the burden of antimicrobial resistance is now very high.23 It is unclear
whether, in the surveyed children, this high level of use of broad-
spectrum antibiotics was indeed justified by local resistance
Africa (n¼245)

patterns, due to the absence of linked local neonatal and paediatric

antimicrobial resistance data. However, the high level of empirical
meropenem

antibiotic use may indicate that at least a proportion of this pre-

gentamicin

6.9 cefotaxime
cefuroxime

cloxacillin
ampicillin

scribing may be inappropriate. Such inappropriate use was found

by Levy et al. 24 in PICUs and paediatric wards, which the authors
attributed to failure to discontinue or de-escalate therapy. Even
in resource-limited settings, where de-escalation may be less com-
7.5

4.2
10.2

7.2

3.9

3.0
1.8
3.3

1.8
18.4
12.7
10.2

Grey shading indicates drug utilization 75% (DU75%) by UN region.

monly considered and where bacteriological cultures are much less

Europe (n ¼332)

frequently performed, successful de-escalation of carbapenems

amoxicillin/inhib.
piperacillin/inhib.
Western

2.8 ampicillin/inhib.

has been reported.25 Therefore, to limit microbial selection pres-

2.8 meropenem

sure, de-escalation upon culture results should be implemented

7.0 vancomycin

4.4 tobramycin
gentamicin 23.6 gentamicin
vancomycin 9.8 cefotaxime

1.6 cefuroxime
meropenem 5.2 amoxicillin

imipenem
29.5 ampicillin

whenever possible.26
3.6 amikacin

We identified several other potential indicators to assess anti-

microbial prescribing that could be used to set benchmarks for
quality improvement of antibiotic use in children and neonates.
Europe (n ¼386)

The simple prevalence of antibiotic use by ward, by hospital or at

national level could be used as a quality indicator if prescription
Southern

1.2 ceftazidime
2.8 cefotaxime
ceftriaxone

2.4 teicoplanin

rates are much higher than in other comparators as part of a

2.4 netilmicin
ampicillin

amikacin

benchmarking programme. The worldwide prevalence rate of anti-

microbial prescribing among children’s wards was 36.7%, with high
rates observed in PICUs (61%) and on surgical wards (35%), which
inhib., enzyme inhibitor.

were twice as high compared with the ESAC 2009-PPS (PICUs, 30%;
5.0
28.2

4.3
4.2
29.1

10.8

child surgical wards, 16%).9 Setting crude prevalence quantitative

targets at the hospital level is very difficult because antibiotic use
amoxicillin/inhib.
Europe (n¼674)

benzylpenicillin

metronidazole

depends on many variables, including patient case-mix, type of

meropenem
flucloxacillin
vancomycin
gentamicin

cefotaxime

hospital, proportion of HAIs and prevalence of resistance. For

amoxicillin

amikacin
Northern

instance, 80% of the centres taking part in this ARPEC-PPS were ter-
tiary care hospitals, with several specialized stand-alone paediatric
hospitals. Therefore, we collected data from a high number of
a

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 Global Point Prevalence Survey in hospitalized children in 2012 JAC
Table 5. Top 10 most-recorded reasons to treat children (.1 month) and neonates (,30 days)

Reason to treat (children) % Reason to treat (neonates) %

Bacterial lower respiratory tract infection 18.7 sepsis 36.4

Prophylaxis for medical problems 15.1 prophylaxis for maternal risk factors 12.2
Prophylaxis for surgical disease 9.9 prophylaxis for newborn risk factors 11.3
Sepsis 9.0 lower respiratory tract infection 8.7
Treatment for surgical disease 6.1 prophylaxis for surgical disease 5.4
Urinary tract infection (upper and lower) 5.6 prophylaxis for medical problems 5.1
Febrile neutropenia/fever in oncologic patients 4.8 catheter-related bloodstream infection 3.4
Upper respiratory tract infection 4.6 CNS infections 3.2
Skin/soft tissue infections 4.4 treatment for surgical disease 2.6
Viral lower respiratory tract infection 3.7 skin/soft tissue infections 2.6

Table 6. Antibiotic use by indication, type of treatment (empirical versus targeted) and UN region for children .1 month

Therapeutic use

community-acquired infection hospital-acquired infection Prophylactic use

empirical targeted empirical targeted medical surgical

Region n % n % n % n % n % n %

Europe 2073 81.8 461 18.2 676 69.9 291 30.1 768 63.3 445 36.7
Africa 343 81.7 77 18.3 54 76.1 17 23.9 27 96.4 1 3.6
Asia 411 72.4 157 27.6 138 60.8 89 39.2 124 42.9 165 57.1
Australia 201 73.1 74 26.9 54 56.8 41 43.2 79 56.4 61 43.6
Latin America 167 73.9 59 26.1 149 69.0 67 31.0 42 48.3 45 51.7
North America 149 70.6 62 29.4 66 68.0 31 32.0 119 71.7 47 28.3

Total 3344 79.0 890 21.0 1137 68.0 536 32.0 1159 60.3 764 39.7

Sixty-eight antibiotics were recorded with unknown indication.

Table 7. Antibiotic use by indication, type of treatment (empirical versus targeted) and UN region for neonates ,30 days

Therapeutic use

community-acquired infection hospital-acquired infection Prophylactic use

empirical targeted empirical targeted medical surgical

Region n % n % n % n % n % n %

Europe 665 91.7 60 8.3 275 77.2 81 22.8 236 76.1 74 23.9
Africa 148 72.2 57 27.8 26 76.5 8 23.5 2 28.6 5 71.4
Asia 108 92.3 9 7.7 103 73.6 37 26.4 122 80.3 30 19.7
Australia 44 100 — — 23 71.9 9 28.1 41 89.1 5 10.9
Latin America 6 75.0 2 25.0 10 58.8 7 41.2 37 86.0 6 14.0
North America 14 93.3 1 6.7 17 94.4 1 5.6 8 53.3 7 46.7

Total 985 88.4 129 11.6 454 76.0 143 24.0 446 77.8 127 22.2

Fourteen antibiotics were recorded with unknown indication.

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 Versporten et al.
children receiving specialized care admitted to, e.g. haematology/
oncology and transplant wards as well as very low birth weight
neonates who were admitted to level 3 NICUs. This could explain
the high overall antibiotic prescribing rates. There is a need to fur-
ther develop the data collection with more hospitals, reducing the
selection bias and stratifying for hospital type and case-mix to
develop more appropriate benchmarking standards.
The early switch from parenteral to oral therapy is another
quality indicator, due to its many advantages, such as decreased
risk of catheter-related infections, reduced costs and the possibil-
ity of early discharge from hospital.27,28 However, it is not known
to what extent different antibiotic administration routes have an
impact on antimicrobial resistance.29 Parenteral administration
among children was more frequent in Asia, Latin America and
Europe (88%, 81% and 67%, respectively) compared with adults
in Europe in the ESAC-PPS (60%).8 The concept of early switching
from parenteral to oral therapy seems uncommon among chil-
dren28 and could be explained by more limited options for oral
broad-spectrum antibacterial equivalents with appropriate formu-
lations, class and potency and the challenges of oral administration
of medications in young children in general.30 A parenteral-to-oral
switch-over programme in line with available guidance can, how-
ever, be introduced into clinical practice28 and should be supported
by collecting information for particular indications in children.31
A further key quality indicator is documentation of the reason
for prescription in the medical notes of the patient, which was
slightly less in European children (76%) than in European adults
(80%),8 but considerably lower in Latin America (52%). Good
documentation of the indication in the patient chart ensures com-
munication of diagnosis and treatment among clinicians, phar-
macists and other healthcare providers, and allows subsequent
prescription review and interventions such as de-escalation and
stopping of antimicrobial treatment. This ESAC-PPS indicator
was used to set a benchmark of .95% in Scottish hospitals.11
Another potential quality indicator is the administration of
antibiotics for surgical prophylaxis. We proposed an international
benchmark of 100% for surgical prophylaxis prescriptions being
administered ,24 h,7 because the duration of surgical prophylaxis
should not exceed a 24 h perioperative period unless exceptional
cases.32 Therefore, the excessively lengthy surgical prophylaxis
for .24 h observed in many hospitals participating in this survey
(up to 84% in Latin America hospitals) is not acceptable. Moreover,
in these hospitals we observed high broad-spectrum surgical pro-
phylactic prescribing, mainly ceftriaxone, which could be explained
by the concern about increasing resistance to first- and second-
generation cephalosporins among Gram-negative isolates. In other
parts of the world, mostly first- and second-generation cephalospor-
ins were administered. Equally concerning is the high proportion of
antibiotics prescribed for medical prophylaxis in all regions except
Africa, including high levels of neonatal medical prophylaxis.
Indeed, medical prophylaxis was the second most common reason
for antibiotic treatment in children, accounting for 15% of all pre-
scriptions. Whether this is an area for quality improvement needs
to be further explored with more detailed evaluation of patterns of
prophylactic antibiotic use and their relation to available evidence.
Study strengths and limitations
The strength of our study lies in the uniformity of data collection,
the simplicity of the protocol and data collection templates (less
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time consuming); and the assurance of data quality (data com-
pleteness and validation process) as described in Versporten
et al. 13 The limitations of this study are inherent to the epidemio-
logical method of a cross-sectional survey.13 Additionally, as
mentioned above, the recruitment of hospitals, mainly done
through existing paediatric or other networks, involving a high
number of highly specialized or referral hospitals, will have
induced selection bias and may partially explain the high anti-
microbial prevalence rates observed. This indicator is strongly
associated with patient characteristics. However, it does not
necessarily explain some worrying findings with respect to quality
indicators, such as the low frequency of documenting the reason
for treatment in the medical files or prolonged antibiotic prescrib-
ing for surgical prophylaxis. These quality indicators should be met
independently of institutional characteristics. Finally, we do not
suspect social desirability bias. We dealt with highly motivated
infectious disease specialists or other, related specialists who
often perform a supervisory function at hospital level. We also
clearly communicated in different ways that they needed to com-
plete the forms with information, which was written down in
medical or other files, without discussing the appropriateness of
the prescribed antimicrobial.
The 2015 WHO global action plan on antimicrobial resistance
proposes collection and reporting of data on the use of antimicro-
bial agents so that trends can be monitored and the impact of
action plans assessed, but does not specifically mention the diffi-
culties of data collection and analysis in children.33 Our ARPEC-PSS
tool constituted a simple method to collect antimicrobial prescrib-
ing data electronically. The uniformity of data collection together
with the implemented online quality assurance improves the val-
idity of the data we collected worldwide. This is of great value to
public health nationally and globally as these methods can be
implemented and repeated regionally in the future.34 It can also
provide meaningful educational feedback to prescribers, which
could have a significant effect on prescribing practices. We have
now identified several measurable quality indicators that could
be used to set benchmarks for antibiotic prescribing in neonates
and children. The next step is to implement feasible quality tar-
gets through repeated PPSs (e.g. quarterly) on a sample of
patients or wards within the same hospitals. This will allow the
future prospective assessment of intervention plans aimed at
improving the quality of antibiotic prescribing.
Acknowledgements
We would like to thank all colleagues who contributed to the success of
this project: Graciela Maria Calle, Hospital de Pediatria Juan P. Garrahan,
Buenos Aires, Argentina; Julia Clark, Royal Children’s Hospital, Brisbane,
Australia; Celia Cooper, Women’s and Children’s Hospital, North
Adelaide, Australia; Christopher C. Blyth and Joshua Reginald Francis,
Princess Margaret Hospital for Children, Perth, Australia; Jameela
Alsalman, Salmaniya Medical Complex, Manama, Bahrain; Hilde Jansens
and Ludo Mahieu, University Hospital Antwerp, Antwerp, Belgium; Paul
Van Rossom, General Hospital Klina, Brasschaat, Belgium; Wouter
Vandewal, AZ Sint Lucas, Brugge, Belgium; Philippe Lepage and Sophie
Blumental, Hôpital Universitaire des Enfants Reine Fabiola, Brussels,
Belgium; Caroline Briquet, Université Catholique de Louvain, Cliniques
Universitaires Saint-Luc, Brussels, Belgium; Dirk Robbrecht, General
Hospital A. Z. Damiaan, Ostend, Belgium; Pierre Maton, NICU-CHC St
Vincent, Rocourt, Belgium; Patrick Gabriels, Sint-Trudo Ziekenhuis,
 Global Point Prevalence Survey in hospitalized children in 2012
Sint-Truiden, Belgium; Zana Rubic and Tanja Kovacevic, University Hospital
Centre Split, Croatia; Jens Peter Nielsen, Pediatric Department,
Regionshospital Viborg, Viborg, Denmark; Jes Reinholdt Petersen,
Department of Neonatology, Rigshospitalet, University of Copenhagen,
Copenhagen, Denmark; Porntiva Poorisrisak, Department of Pediatrics,
Naestved Hospital, Naestved, Denmark; Lise Heilmann Jensen, Roskilde
University Hospital, Roskilde, Denmark; Mari Laan, Tallinn Children’s
Hospital, Tallinn, Estonia; Eda Tamm, Children’s Clinic of Tartu University
Hospital, Tartu, Estonia; Maire Matsinen and Maija-Liisa Rummukainen,
Central Finland Health Care District, Jyväskylä, Finland; Vincent Gajdos
and Romain Olivier, Hopitaux Universitaires Paris Sud, Antoine Beclere,
Clamart, France; Flore Le Maréchal, Department of Pediatrics and
Neonatology, University Hospital, Dijon, France; Alain Martinot, François
Dubos, Marion Lagrée, CHRU Lille, Lille University Hospital, Lille, France;
Sonia Prot-Labarthe and Mathie Lorrot, AP-HP Hôpital Robert-Debré,
Paris, France; Daniel Orbach, Institut Curie, Paris, France; Karaman
Pagava, Tbilisi State Medical University, Tbilisi, Georgia; Markus Hufnagel,
Division of Pediatric Infectious Diseases and Rheumatology, Center of
Pediatrics and Adolescent Medicine, University Medical Center, Freiburg,
Germany; Markus Knuf, Children’s Hospital, Dr Horst-Schmidt-Kliniken,
Wiesbaden, Germany; Stephanie A. A. Schlag and Johannes Liese,
University Children’s Hospital, University of Würzburg, Würzburg,
Germany; Lorna Renner, Prof. Korle Bu Teaching Hospital, Accra, Ghana;
Anthony Enimil and Marah Awunyo, Komfo Anokye Teaching Hospital,
Kumasi, Ghana; Garyfallia Syridou and Nikos Spyridis, Aglaia Kyriakou
Children’s Hospital, Athens, Greece; Elena Critselis, First University
Department of Pediatrics, ‘Aghia Sophia’ Children’s Hospital, Athens,
Greece; Sofia Kouni and Katerina Mougkou, University of Athens
Collaborative Center for Clinical Epidemiology and Outcome Research,
Athens, Greece; Fani Ladomenou, University Hospital of Heraklion, Crete,
Greece; Despoina Gkentzi, University General Hospital of Patras, Patras,
Greece; Elias Iosifidis and Emmanuel Roilides, 3rd Department of
Pediatrics, Faculty of Medicine, Aristotle University School of Health
Sciences, Hippokration Hospital, Thessaloniki, Greece; Suneeta Sahu,
Microbiology, Apollo Hospitals, Bhubaneswar, Odisha, India; Srinivas
Murki, Fernandez Hospital, Hyderabad, India; Manoj Malviya and Durga
Bhavani Kalavalapalli, Nice Hospital for Women, Newborns and Children,
Hyderabad, India; Sanjeev Singh, Amrita Institute of Medical Sciences,
Kochi, India; Tanu Singhal, Kokilaben Dhirubhai Ambani Hospital and
Medical Research Institute, Mumbai, India; Garima Garg, Escorts Heart
Institute, New Delhi, India; Pankaj Garg, Sir Ganga Ram Hospital,
Rajinder Nagar, New Delhi, India; Neelam Kler, Sir Ganga Ram Hospital,
Rajinder Nagar, New Delhi, India; Jafar Soltani, Besat Tertiary Hospital
affiliated to Kurdistan University of Medical Sciences, Sanandaj,
Kurdistan, Iran; Zahra Jafarpour and Gholamreza Pouladfar, Professor
Alborzi Clinical Microbiology Research Center, Shiraz University of Medical
Sciences, Shiraz, Iran; Giangiacomo Nicolini, San Martino Hospital,
Pediatric Department, Belluno, Italy; Carlotta Montagnani and Luisa
Galli, Department of Health Sciences, University of Florence, Meyer
Children’s University Hospital, Florence, Italy; Susanna Esposito, Pediatric
Highly Intensive Care Unit, and Rossana Tenconi, Department of
Pathophysiology and Transplantation, Università degli Studi di Milano,
Fondazione IRCCS Ca’ Granda Ospedale Maggiore Policlinico, Milan, Italy;
Andrea, Lo Vecchio, University of Naples Federico II, Naples, Italy;
Daniele Dona’ and Carlo Giaquinto, Department for Woman and Child
Health, Padua, Italy; Eleonora Borgia, University Hospital of Padova,
Padua, Italy; Patrizia D’Argenio and Maia De Luca, Bambino Gesù
Children’s Hospital, Rome, Italy; Chiara Centenari, Paediatric and
Neonatal Unit, Hospital of Viareggio, Viareggio, Italy; Lul Raka, National
Institute of Public Health of Kosovo and University of Prishtina, and
Denis Raka, University of Prishtina, Prishtina, Kosovo; Abeer Omar and
Haifaa Al-Mousa, Directorate of Infection Control, Ministry of Health,
Kuwait City, Kuwait; Dzintars Mozgis, Centre for Diseases Prevention and
Control, Riga, Latvia; Inese Sviestina, University Children’s Hospital, Riga,
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JAC
Latvia; Sigita Burokiene, Children’s Hospital, Affiliate of Vilnius University
Hospital Santariskiu Klinikos, Vilnius, Lithuania; Vytautas Usonis, Vilnius
University, Vilnius, Lithuania; Gabriela Tavchioska, General Hospital ‘Borka
Taleski’, Prilep, Macedonia; Antonia Hargadon-Lowe, Queen Elizabeth
Central Hospital, Blantyre, Malawi; Peter Zarb and Michael A. Borg, Mater
Dei Hospital, Msida, Malta; Carlos Agustı́n González Lozano and Patricia
Zárate Castañon, Instituto Nacional de Pediatrı́a, México D.F., México;
Martha E. Cancino, Universidad Autónoma de Nayarit, México
and DURG-LA (Grupo para la Investigación de la Utilización de los
Medicamentos-América Latina), Tepic, Nayarit, México; Bernadette
McCullagh, South Eastern Health and Social Care Trust, Belfast, Northern
Ireland; Ann McCorry, Southern Health and Social Care Trust, Craigavon,
Northern Ireland; Cairine Gormley, Western Health and Social Care Trust,
Derry, Northern Ireland; Zaina Al Maskari and Amina Al-Jardani, Royal
Hospital, Muscat, Oman; Magdalena Pluta, Department of Children’s
Infectious Diseases, Medical University of Warsaw, Poland, Warsaw,
Poland; Fernanda Rodrigues and Ana Brett, Hospital Pediátrico, Centro
Hospitalar e Universitário de Coimbra, Coimbra, Portugal; Isabel Esteves,
Hospital de Santa Maria, Pediatric Department, Pediatric Infectious
Diseases Unit, Lisbon, Portugal; Laura Marques, Centro Hospitalar do
Porto, Porto, Portugal; Jameela Ali AlAjmi, Hamad Medical Corporation,
Doha, Qatar; Simona Claudia Cambrea, Faculty of Medicine, ‘Ovidius’
University, Constanta, Romania; Asia N. Rashed, King Abdulaziz Medical
City—Jeddah, Jeddah, Saudi Arabia; Aeshah Abdu Mubarak Al Azmi,
Ministry of National Guard Health Affairs, King Abdulaziz Medical City,
Pharmaceutical Care Services Department, Jeddah, Saudi Arabia; Si Min
Chan, Khoo Teck Puat-National University Children’s Medical Institute,
National University Health System, Singapore, Singapore; Mas Suhaila
Isa, National University Hospital, Singapore; Peter Najdenov, General
Hospital Jesenice, Jesenice, Slovenia; Milan Čižman, University Medical
Centre, Ljubljana, Slovenia; Sibila Unuk, University Medical Center
Maribor, Maribor, Slovenia; Heather Finlayson, Department of Paediatrics
and Child Health, Stellenbosch University, Cape Town, South Africa;
Angela Dramowski, Tygerberg Hospital, Cape Town, South Africa; Irene
Maté-Cano, Hospital Universitario del Henares, Coslada, Madrid, Spain;
Beatriz Soto, Hospital Universitario de Getafe, Getafe, Madrid, Spain;
Cristina Calvo, Severo Ochoa Hospital, Leganés, Madrid, Spain; Begoña
Santiago and Jesus Saavedra-Lozano and Amaya Bustinza, Gregorio
Marañon Hospital, Madrid, Spain; Luis Escosa-Garcı́a, Hospital Infantil
Universitario La Paz, Madrid, Spain; Noelia Ureta, Elisa Lopez-Varela and
Pablo Rojo, Hospital Universitario 12 de Octubre, Madrid, Spain; Alfredo
Tagarro, Hospital Universitario Infanta Sofia, San Sebastian de los Reyes,
Madrid, Spain; Pedro Terol Barrero, Hospital Universitario Virgen Macarena,
Seville, Spain; Elena Maria Rincon-Lopez, Hospital Universitario y
Politecnico La Fe, Valencia, Spain; Ismaela Abubakar, Edward Francis Small
Teaching Hospital/Royal Victoria Teaching Hospital, Banjul, The Gambia; Jeff
Aston, Mitul Patel and Alison Bedford Russell, Birmingham Children’s
Hospital NHS Foundation Trust, Birmingham, UK; Maggie Heginbothom,
Public Health Wales, Cardiff, UK; Prakash Satodia, University Hospitals
Coventry and Warwickshire NHS Trust, Coventry, UK; Mehdi Garbash,
County Durham and Darlington NHS Foundation Trust, Durham and
Darlington, UK; Alison Johnson, Wye Valley NHS Trust, Hereford, UK; David
Sharpe, Alder Hey Children’s NHS Foundation Trust, Liverpool, UK;
Christopher Barton, Institute of Child Health, University of Liverpool,
Liverpool, UK; Esse Menson and Sara Arenas-Lopez, Evelina London
Children’s Hospital, London, UK; Suzanne Luck, Kingston Hospital NHS
Foundation Trust, London, UK; Katja Doerholt, St George’s Hospital,
London, UK; Paddy McMaster, North Manchester General Hospital,
Manchester, UK; Neil A. Caldwell, Wirral University Teaching Hospital NHS
Foundation Trust, Merseyside, UK; Andrew Lunn, Nottingham Children’s
Hospital, Nottingham, UK; Simon B. Drysdale, Oxford University Hospitals
NHS Trust, Oxford, UK; Rachel Howe, Peterborough City Hospital,
Peterborough, UK; Tim Scorrer and Florian Gahleitner, Queen Alexandra
Hospital, Portsmouth, UK; Richa Gupta, Royal Preston Hospital, Lancashire
1115
 Versporten et al.
Teaching Hospitals, Preston, UK; Clare Nash, Sheffield Children’s NHS
Foundation Trust, Sheffield, UK; John Alexander, University Hospital of
North Midlands, Stoke on Trent, UK; Mala Raman, Torbay Hospital, South
Devon Health Care NHS Foundation Trust Torquay, UK; Emily Bell, Royal
Cornwall Hospitals NHS Trust, Truro, Cornwall, UK; Veena Rajagopal,
St George’s NHS Trust, London, UK; Stephan Kohlhoff, SUNY Downstate
Medical Center, Brooklyn, USA; Elaine Cox, Kristen Nichols and Elaine Cox,
Riley Hospital for Children at IU Health, Indianapolis, USA; Theoklis Zaoutis,
The Children’s Hospital of Philadelphia, Philadelphia, USA.
Funding
This work was supported by the European Commission Directorate General
for Health and Consumers (DG SANCO) through the Executive Agency for
Health and Consumers ‘(Agreement number—2009 11 01)’ (http://ec.
europa.eu/eahc/). The October – November 2012 Antibiotic Resistance
and Prescribing in European Children Point Prevalence Survey was
co-funded by the Paediatric European Network for Treatment of AIDS
(PENTA) (http://www.penta-id.org/).
Transparency declarations
None to declare.
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