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White Paper: Bridging the gap between surveillance data and antimicrobial stewardship in the outpatient sector—practical guidance from the JPIAMR ARCH and COMBACTE-MAGNET EPI-Net networks

Abstract

Background: The outpatient setting is a key scenario for the implementation of antimicrobial stewardship (AMS) activities, considering that overconsumption of antibiotics occursmainly outside hospitals. This publication is the result of a joint initiative by the JPIAMR ARCH and COMBACTE-MAGNET EPI-Net networks, which is aimed at formulating a set of target actions for linking surveillance data with AMS activities in the outpatient setting. Methods: A scoping review of the literature was carried out in three research areas: AMS leadership and accountability; antimicrobial usage and AMS; antimicrobial resistance and AMS. Consensus on the actions was reached through a RAND-modified Delphi process involving over 40 experts in infectious diseases, clinical microbiology, AMS, veterinary medicine or public health, from18 low-, middle- and high-income countries. Results: Evidence was retrieved from 38 documents, and an initial 25 target actions were proposed, differentiating between essential or desirable targets according to clinical relevance, feasibility and applicability to settings and resources. In the first consultation round, preliminary agreement was reached for all targets. Further to a second review, 6 statements were re-considered and 3 were deleted, leading to a final list of 22 target actions in the form of a practical checklist. Conclusions: This White Paper is a pragmatic and flexible tool to guide the development of calibrated surveillance-based AMS interventions specific to the outpatient setting, which is characterized by substantial inter- and intra-country variability in the organization of healthcare structures, maintaining a global perspective and taking into account the feasibility of the target actions in low-resource settings.

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White Paper: Bridging the gap between surveillance data and antimicrobial stewardship in the outpatient sector—practical guidance from the JPIAMR ARCH and COMBACTE-MAGNET EPI-Net networks

Author: Arieti, Fabiana; Göpel, Siri; Sibani, Marcella; Carrara, Elena; Pezzani, Maria Diletta; Murri, Rita; Mutters, Nico T.; López Cerero, Lorena; Voss, Andreas; Cauda, Roberto; Tacconelli, Evelina
Publisher: Oxford Academic
Year: 2020
DOI: 10.1093/jac/dkaa428
Source: https://idus.us.es/bitstreams/b0b3e709-fa38-48cd-8165-511f6c6ceece/download
Whi e Pape : B idging he gap be ween su eillance da a and
an imic obial s ewa dship in he ou pa ien sec o —p ac ical
guidance om he JPIAMR ARCH and COMBACTE-MAGNET
EPI-Ne ne wo ks
Fabiana A ie i
1
†, Si i Go¨pel
2,3
†, Ma cella Sibani
1
*, Elena Ca a a
1
, Ma ia Dile a Pezzani
1
, Ri a Mu i
4
,
Nico T. Mu e s
5
, Lo ena Lo`pez-Ce e o
6
, And eas Voss
7
, Robe o Cauda
4
and E elina Tacconelli
1,2,3
on behal o
he ARCH wo king g oup‡
1
In ec ious Diseases Sec ion, Depa men o Diagnos ics and Public Heal h, Uni e si y o Ve ona, Ve ona, I aly;
2
In ec ious Diseases,
Depa men o In e nal Medicine I, Tu¨bingen Uni e si y Hospi al, Tu¨bingen, Ge many;
3
Ge man Cen e o In ec ion Resea ch (DZIF),
Clinical Resea ch Uni o heal hca e associa ed in ec ions, Tu¨bingen, Ge many;
4
Ins i u e o In ec ious Diseases, Fondazione Policlinico
Uni e si a io A. Gemelli IRCCS, Uni e si a´ Ca olica del Sac o Cuo e, Rome, I aly;
5
Ins i u e o Hygiene and Public Heal h, Bonn
Uni e si y Hospi al, Bonn, Ge many;
6
Mic obiology and In ec ious Diseases Uni , Uni e si y Hospi al Vi gen Maca ena, Se illa, Spain;
7
Depa men o Clinical Mic obiology and In ec ious Diseases, Canisius-Wilhelmina Hospi al, Nijmegen, The Ne he lands
*Co esponding au ho . E-mail: ma cella.sibani@uni .i
†Equally con ibu ing i s au ho s.
‡Membe s a e lis ed in he Acknowledgemen s sec ion.
Backg ound: The ou pa ien se ing is a key scena io o he implemen a ion o an imic obial s ewa dship
(AMS) ac i i ies, conside ing ha o e consump ion o an ibio ics occu s mainly ou side hospi als. This publica-
ion is he esul o a join ini ia i e by he JPIAMR ARCH and COMBACTE-MAGNET EPI-Ne ne wo ks, which is
aimed a o mula ing a se o a ge ac ions o linking su eillance da a wi h AMS ac i i ies in he ou pa ien
se ing.
Me hods: A scoping e iew o he li e a u e was ca ied ou in h ee esea ch a eas: AMS leade ship and accoun -
abili y; an imic obial usage and AMS; an imic obial esis ance and AMS. Consensus on he ac ions was eached
h ough a RAND-modi ied Delphi p ocess in ol ing o e 40 expe s in in ec ious diseases, clinical mic obiology,
AMS, e e ina y medicine o public heal h, om 18 low-, middle- and high-income coun ies.
Resul s: E idence was e ie ed om 38 documen s, and an ini ial 25 a ge ac ions we e p oposed, di e en ia -
ing be ween essen ial o desi able a ge s acco ding o clinical ele ance, easibili y and applicabili y o se ings
and esou ces. In he i s consul a ion ound, p elimina y ag eemen was eached o all a ge s. Fu he o a se-
cond e iew, 6 s a emen s we e e-conside ed and 3 we e dele ed, leading o a inal lis o 22 a ge ac ions in
he o m o a p ac ical checklis .
Conclusions: This Whi e Pape is a p agma ic and lexible ool o guide he de elopmen o calib a ed
su eillance-based AMS in e en ions speci ic o he ou pa ien se ing, which is cha ac e ized by subs an ial in-
e - and in a-coun y a iabili y in he o ganiza ion o heal hca e s uc u es, main aining a global pe spec i e
and aking in o accoun he easibili y o he a ge ac ions in low- esou ce se ings.
In oduc ion
An imic obial s ewa dship (AMS) in he ou pa ien se ing is a c i ic-
al aspec wi hin a global scena io o he con inuous inc ease in
an imic obial esis ance (AMR) and o e consump ion o an ibio ics,
which mainly occu s (app oxima ely 80%–90%) ou side hospi-
als.
1–3
Hence, i is impossible o hypo hesize any AMS in e en ion
in he ou pa ien se ing wi hou he abili y o adequa ely ack
an imic obial use (AMU) and AMR. This p ocess can be done in se -
e al ways, om single p esc ibing uni s o la ge e i o ial a eas,
and should be able o gua an ee eedback o indi idual p esc ibe s
and allow benchma king wi h egional and na ional da a. Due o
V
CThe Au ho (s) 2020. Published by Ox o d Uni e si y P ess on behal o he B i ish Socie y o An imic obial Chemo he apy.
This is an Open Access a icle dis ibu ed unde he e ms o he C ea i e Commons A ibu ion Non-Comme cial License (h p://c ea i ecom
mons.o g/licenses/by-nc/4.0/), which pe mi s non-comme cial e-use, dis ibu ion, and ep oduc ion in any medium, p o ided he o iginal
wo k is p ope ly ci ed. Fo comme cial e-use, please con ac [email p o ec ed]
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doi:10.1093/jac/dkaa428
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he ele ance o hese da a, many e o s ha e been unde aken
a he in e na ional le el (WHO, ESAC ECDC, Canadian
An imic obial Resis ance Su eillance Sys em, Japanese
An imic obial Consump ion Su eillance) o s anda dize epo ing.
Howe e , he he e ogenei y o me ics o AMU su eillance, espe-
cially o he ou pa ien se ing, makes i di icul o o mula e clea
ecommenda ions on which me ic should bep e e ed.
4
While many AMS in e en ions ocus on educing consump ion,
i is impo an o poin ou ha in many se ings he AMS p o-
g amme is de eloped o educe AMR. In he ou pa ien se ing, a
numbe o ini ia i es (i.e. educa ional ools and awa eness cam-
paigns) ha e been p o ed o be success ul in enhancing app op i-
a eness o p esc ip ions. Howe e , al hough good examples o
bo om-up AMS ini ia i es in eg a ed in o ou pa ien daily clinical
p ac ice a e inc easingly being desc ibed,
5
high-quali y e idence
da a showing he impac o such ini ia i es on mic obiological ou -
comes a e s ill limi ed, mainly because o sca ce and he e oge-
neous epo ing o da a.
6
Indeed, when i comes o he o he pilla
o AMS in e en ions (i.e. moni o ing AMR), he ou pa ien se ing is
e en mo e challenging because mos he apeu ic decisions a e
made empi ically. Mic obiological da a, when a ailable, a e di i-
cul o in e p e and a e a ely ep esen a i e o he gene al
popula ion.
Despi e he a ailabili y o guidelines o implemen a ion and
managemen o AMS p og ammes in he communi y (CDC Co e
Elemen s and Field Guide, SHEA MITIGATE o Eme gency
Depa men and U gen Ca e, Join Commission An imic obial
S ewa dship Ambula o y Ca e), p ac ical ecommenda ions on
how p esc ibe s should ela e o local mic obiological and con-
sump ion da a o imp o e p esc ip ions a e a ely discussed.
Undoub edly, in a con ex whe e each coun y has i s own legisla-
ion egula ing bo h an ibio ic policies and ou pa ien en i ies, i is
di icul o issue widely applicable ecommenda ions. The ou -
pa ien se ing can be an elusi e concep o ou line and se e al
de ini ions a e ound in he li e a u e (Table1); addi ionally, i s o -
ganiza ion has been con inuously and apidly changing in ecen
decades, e en in low- and middle- income coun ies (LMICs).
7,8
Fo he pu poses o his esea ch pape , JPIAMR ARCH and
COMBACTE-MAGNET EPI-Ne
9,10
ha e ha monized e o s o
ou line a s uc u ed app oach ha p o ides a se o ac ions o
acili a e an ibio ic policy in e en ions and d i e he link be ween
su eillance da a on AMR and an ibio ic consump ion and imple-
men a ion o AMS ac i i ies.
The in e na ional expe panel has p oduced a se ies o Whi e
Pape s ocused on ou di e en se ings: hospi al; ou pa ien ;
long- e m ca e acili ies (LTCFs); and e e ina y. The esea ch
ques ions ha cons i u e he e idence base o he ecommenda-
ions ocused on h ee main a eas: (i) leade ship commi men ,
accoun abili y and AMS eam; (ii) AMU and AMS; and (iii) AMR and
AMS. The inal lis o a ge ac ions summa izes he epidemiologic-
al, mic obiological and an imic obial da a ha a e essen ial o
an ibio ic p esc ibing and policy. The en i e p ocess was unde -
pinned by a s ong ocus on he easibili y o he ac ions and he
One Heal h app oach. This pape ocuses on he ou pa ien se ing,
namely any ca e se ice p o ided o pa ien s who a e no admi -
ed oa hospi al o LTCF, anging om immedia e ea men o an
acu e and o en se ious illness (e.g. eme gency ou pa ien clinics)
o ou pa ien special y clinics and p ima y heal h ca e acili ies
ha p o ide p e en i e and cu a i e se ices (Table 1). The
in ended audience o his Whi e Pape is heal hca e p o essionals
and leade s wo king in ou pa ien clinics in high-income coun ies
who a e willing o es ablish o implemen an e ec i e AMS p o-
g amme; howe e , speci ic e e ences o LMICs a e also p o ided
whene e easible and ele an . The checklis s p oduced a e
a ailable o download on he ARCH websi e,
9
and can be used as
p ac ical ools by heal h p o essionals and policymake s o es ab-
lish and/o moni o s ewa dship ac i i ies. Dissemina ion will be
ensu ed by he ne wo ks in ol ed in he JPIAMR ARCH p ojec ha
a e lis ed in Table 1o he i s pape in his se ies.
11
Me hods
Using a One Heal h app oach, he p esen p ojec was concei ed o de elop
expe consensus based on e alua ion o he a ailable li e a u e and guid-
ance documen s on AMS and su eillance. This was ollowed by he de el-
opmen o a i s d a o a ge s and a RAND-modi ied Delphi p ocess o
he de ini i e alida ion o a ge s (p o ocola ailable a he ARCHwebsi e).
9
The en i e p ocess is desc ibed in he i s pape o his se ies, which ocuses
on he hospi al se ing.
11
B ie ly, he p ocess in ol ed he ollowing: de el-
opmen o key esea ch ques ions (lis ed in Table3o he i s Whi e Pape
o his se ies) de i ing om a sys ema ic e iew p e iously de eloped o
p o ide guidance on he AMR su eillance modali ies ha a e bes sui ed o
d i ing s ewa dship in e en ions in hospi als (EPI-Ne COACH p ojec );
12
a
na a i e e iew o he a ailable e idence; he p oduc ion o a i s d a o
a ge s p o ided o he expe s in a web-based su ey in which ag eemen
was exp essed on a nine-poin Like scale; a 2 day ace- o- ace mee ing
held a he end o Oc obe 2019. Fo he li e a u e sea ch, ele an publica-
ions in English, published in he las 10yea s, we e sc eened wi h a s ep-
wise app oach: i s , guidance ( om scien i ic socie ies, in e na ional and
na ional au ho i ies) and documen s included in he EU-JAMRAI eposi-
o y
13
we e assessed, and hen he sea ch was ca ied ou using MEDLINE
(Na ional Lib a y o Medicine, Be hesda, MD, USA) wi h a combina ion o he
ollowing e ms: an imic obial, consump ion, ou pa ien , an imic obial d ug
esis ance and su eillance.
Nex , du ing he ace- o- ace mee ing, he expe s we e p esen ed wi h
a summa y o he e idence, discussed he esul s o he online su ey and
inalized he lis o a ge s. Recommenda ions, s a e o he a , and o iginal
app oaches we e e alua ed by ocusing on easibili y and adap abili y o
di e en economic and heal hca e con ex s o compile a lis o ‘essen ial’
and ‘desi able’ a ge s. Ta ge s we e ecognized as ‘essen ial’ when widely
Table 1. De ini ions o ou pa ien se ings
Re e ence De ini ion
59 An ou pa ien is a pe son who goes o a heal hca e acil-
i y and who lea es he acili y wi hin 3 h o he s a o
consul a ion. An ou pa ien is no o mally admi ed o
a acili y.
60 Ca e p o ided in acili ies whe e pa ien s do no emain
o e nigh (e.g. hospi al-based ou pa ien clinics, non--
hospi al-based clinics and physician o ices, u gen
ca e cen es, ambula o y su gical cen es e c.).
61
a
Any ca e se ice p o ided o pa ien s who a e no admi -
ed as inpa ien s o a hospi al.
a
Fo he pu poses o his documen , we conside ed his b oad de ini ion
o ou pa ien se ing; howe e , mos o he e idence ound in he li e a-
u e e iew was ela ed o GP clinics, amily physician clinics and paedia -
ic clinics.
Linking su eillance wi h AMS in he ou pa ien se ing JAC
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p ac icable i no al eady b oadly accomplished, and ‘desi able’ in he case
o limi ed easibili y o esou ce cons ain s. Topics o which mo e e idence
was equi ed in o de o d aw up ecommenda ions we e de inedas p io i y
opics o u u e esea ch. A o al o 40 expe s om 18 coun ies and 30
ne wo ks de eloped he p o ocol, con ibu ed o eaching a consensus and
app o ed he inal lis o indica ions (see i s pape in his se ies).
Resul s
A o al o 38 documen s we e included o he app aisal,
2,6,14–49
co e ing all egions wo ldwide; howe e , he majo i y (32, 84%)
we e om Eu ope, No h Ame ica o he Eas Asia and Paci ic
egions. Mos o he e idence was e ie ed om guidelines, sys-
ema ic e iews, p ac ical guides o ools, s udies and su eillance
epo s, mos ly encompassing adul and paedia ic se ings.
A limi ed numbe o expe opinion and s udy p o ocol documen s
we e also included.
E idence o he leade ship commi men , accoun abili y and
AMS eam esea ch a ea was e ie ed om 10 guidelines, 3 sys-
ema ic e iews and 1 s udy p o ocol, while e idence ela i e
o AMU and AMS was ob ained om 8 guideline documen s, 6
e iews, 13 s udy a icles o epo s, 3 p ac ical ools and 1 expe
opinion. No guidelines speci ically add essing AMR and AMS we e
iden i ied, and e idence o his opic was e ie ed om eigh
documen s, including e iews, s udies, a ew p ac ical ools and
expe opinion.
P elimina y s a emen s o he h ee a eas o esea ch (leade -
ship commi men , accoun abili y and AMS eam; AMU and AMS;
and AMR and AMS) we e es ablished. Twen y expe s a ed he ini-
ial s a emen s h ough an online su ey and ag eemen was
eached o all o hem; howe e , du ing he ace- o- ace mee ing
(Oc obe 2019) some aspec s we e discussed u he : 6 s a e-
men s we e e-conside ed and e-ph ased and 3 we e dele ed,
leading o a lis o 22 a ge ac ions ha we e app o ed in hei
inal e sion by he en i e panel. Tables2–4, espec i ely, lis he
ecommended a ge s o he h ee a eas o esea ch. Due o lack
o e idence o expe ag eemen , i was no possible o o mula e
a ge s on one esea ch ques ion o AMU and AMS and on h ee
esea ch ques ions o AMR and AMS, highligh ing he gaps in he
li e a u e and expanding he lis o esea ch p io i ies (Table 5).
Discussion
Leade ship commi men , accoun abili y and
an imic obial s ewa dship eam
The ou pa ien se ing is cha ac e ized by consis en in e - and
in a-coun y a iabili y in he o ganiza ion o heal hca e s uc-
u es, which e lec s he complexi y in he design o AMS
p og ammes. Ne e heless, i is c ucial o iden i y a clea leade
(o leade s) o guide he AMS eam and ac i i ies.
19,50
In la ge ad-
minis a i e se ings such as ou pa ien clinics, an o ganiza ional
s uc u e ollowing he ‘hub and spoke’ model can be conside ed.
Fo example, in he case o an ou pa ien se ice linked o a hos-
pi al, esou ces such as he mic obiology labo a o y, pha macy, IT
s uc u e and guidance by in ec ious disease specialis s can be
used o d i e AMS ac i i ies, while in low-income coun ies exis ing
p og ammes such as hose o HIV, mala ia and ube culosis can
be in eg a ed wi h AMS o sa e esou ces. By con as , in he case
o smalle p esc ibing uni s such as single GPs, den is s o o he
special ies, a clea AMS leade should be iden i ied o each uni .
The wo king g oup highligh ed he c ucial ole o se e al di e en
p o essionals wi hin he ou pa ien se ing. GPs a e necessa ily he
pi o s o mos AMS ac i i ies in his se ing; howe e , depending on
he esou ces and speci ic cha ac e is ics, leading oles can be
assigned o o he physicians, a physician’s assis an , an ad anced
p ac ice egis e ed nu se o a pha macis . The inclusion o a dis ic
pha macis can be a key elemen o deli e messages o pa ien s
and physicians,
21,51
especially, bu no only, in low- esou ce se -
ings and in coun ies wi h a high p opo ion o unp esc ibed
Table 2. Leade ship commi men , accoun abili y and an imic obial s ewa dship eam in he ou pa ien se ing
Pa icipan s in he an imic obial s ewa dship eam
1.1. Essen ial
The AMS eam should be mul idisciplina y. Co e membe s should include leade s wi h expe ience in AMS and su eillance, a ep esen a i e o pha -
macies in he local dis ic and a ep esen a i e o gene al p ac i ione s.
1.2. Desi able
Include addi ional igu es in he co e g oup acco ding o he se ing, esou ces and ype o in e en ion (i.e. o he specialis s om a ge wa ds, in ec-
ion con ol nu ses and IT expe s).
Ins i u ional suppo o he o ganiza ion and managemen o an imic obial s ewa dship p og ammes: legal amewo k
1.3. Essen ial
Regula e and p omo e AMS ac i i ies a e e y le el o heal hca e o ganiza ion wi h well-de ined oles, esponsibili ies and a clea go e nance
s uc u e.
Ins i u ional suppo o he o ganiza ion and managemen o an imic obial s ewa dship p og ammes: s a ing pe sonnel
1.4. Essen ial
Include dedica ed ime and speci ic sala y suppo o AMS ac i i ies as pa o AMS p og ammes.
1.5. Essen ial
Alloca e ull- ime equi alen s acco ding o na ional equi emen s o he di e en se ings and le el o in e en ion, whe e a ailable.
A ie i e al.
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an ibio ic sales whe e pha macies and o he p i a e d ug s o es
ep esen he p ima y access poin s o an imic obials.
52
O he po-
en ial pa ne s, especially in he case o smalle adminis a i e
uni s, can be local heal hca e depa men s, heal h insu ance com-
panies, heal hca e p o essional socie ies, local mic obiology labo-
a o ies and LTCFs. In LMICs, he in eg a ion o AMS e o s in o
Table 3. An imic obial usage and an imic obial s ewa dship in he ou pa ien se ing
Which an ibio ics should be moni o ed?
2.1. Essen ial
Include as minimum equi emen s o moni o ing:
- o e all consump ion o an ibio ics
- IV and o al an ibio ics used in high olumes o acco ding o he local anking (5–10 mos used agen s)
- an imic obials included in he Wa ch and Rese e ca ego ies WHO Essen ial D ug Lis AWARE index
- an ibio ics used o ea ing in ec ions caused by locally clinically ele an esis an pa hogens as de ined by he AMS eam
2.2. Desi able
Moni o he o al consump ion o sys emic an imic obials (ATC J01 class), bo h IV and o al o mula ions, as o e all agg ega ed da a and as sub-
classes o indi idual agen s.
2.3. Desi able
S a i y da a by p esc ibing medical special y (i.e. gene al p ac i ione , paedia ician, den is ) o allow o benchma king. Ta ge indica ions/
synd omes o which an ibio ics should be moni o ed:
- Respi a o y ac in ec ion (RTI), including uppe and lowe RTI
- U ina y ac in ec ion
- Dia hoea (depending on local epidemiology and ele ance)
- Sexually ansmi ed diseases
- Skin and so issue in ec ions
Which me ics should be employed?
2.4. Essen ial
Fo na ional/ egional su eillance, moni o DDDs pe 1000 inhabi an s pe day and numbe o p esc ip ions pe 1000 inhabi an s pe yea
2.5. Essen ial
Fo su eillance a he p esc ibe le el, moni o numbe o p esc ip ions ei he pe 100 pa ien s/yea o 100 pa ien con ac s/yea
2.6. Desi able
Fo na ional/ egional su eillance, moni o numbe o p esc ip ions pe 100 physician con ac s/yea
2.7. Desi able
Fo su eillance a he p esc ibe le el, moni o DDD pe 100 pa ien s pe yea
2.8. Desi able
Fu he me ics should be based on logis ics and he ypes o An imic obial S ewa dship in e en ions ha will be implemen ed; o in e en ions a -
ge ing o e -p esc ip ion o speci ic diagnoses, moni o p esc ip ion a e o speci ic diagnoses [p esc ip ion/indica ion/p esc ibe /yea (mon h)].
Repo deli e y
2.9. Essen ial
Make local agg ega ed da a a ailable o physician ne wo ks and speci ic p esc ibing uni s. S a i ica ion by special y o indica ion should be done
whene e possible.
2.10. Desi able
I consump ion da a b oken down by single p esc ibe ac i i y (i.e. numbe o DDDs o p esc ip ions a ibu able o each indi idual gene al p ac i ione
o o he p esc ibe s) a e a ailable, deli e hem o he speci ic p esc ibing uni s, making hem a ailable o p esc ibe s and ca egi e s, bu also o
adminis a ion. Pe o m u he agg ega ion by special y o s a i ica ion by indica ion whene e possible.
Which ime in e al should be used o epo ing?
2.11. Essen ial
P o ide an imic obial consump ion da a on a egula basis, a leas annually.
2.12. Desi able
The da a should be agg ega ed a leas qua e ly o allow o desc ibing seasonal a ia ion in ends in high-usage indica ions o espi a o y
in ec ions.
Linking su eillance wi h AMS in he ou pa ien se ing JAC
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well-es ablished s uc u es o su eillance and ea men o com-
municable diseases such as HIV, mala ia and ube culosis was
iden i ied by he panel as a s a egy o use in he implemen a ion
o AMS ac i i ies.
In e ms o ins i u ional suppo h ough a legal amewo k,
he a ailable li e a u e mos ly ocuses on he ele ance o he
commi men o public heal h au ho i ies in p omo ing AMS
and communica ing wi h pa ien s and heal hca e p o essionals,
iden i ying AMS coo dina o s a a local le el and including AMS-
ela ed du ies wi hin job desc ip ions.
19,22,25,50
Some coun ies, o
example, ha e implemen ed inancial incen i es o p ima y ca e
p o ide s. Pay- o -pe o mance sys ems a e implemen ed wi hin
he UK’s Na ional Heal h Se ice, he na ional heal h se ice in
F ance and he heal hca e sys em in he USA.
An imic obial usage and an imic obial s ewa dship
The a ailable guidance on AMS in he ou pa ien se ing sugges s
moni o ing p esc ip ions o condi ions ypically associa ed wi h a
high a e o inapp op ia e p esc ibing wi hou indica ing speci ic
pha maceu ical ca ego ies. Cu en ly, mos high-income coun ies
and an inc easing numbe o LMICs ha e da a lows om eim-
bu semen o sales eco ds ha can p o ide da a o na ional o
in e na ional su eillance sys ems. Pe iodic epo s o elec onic
ools allow open consul a ion o hese su eillance da a a
he coun y o egional le el,
27,31
wi h he addi ional possibili y o
acking consump ion o sys emic an ibio ics (ATC J01) in dis inc
hospi als and communi ies. In some cases, he da a can be also
b oken down o J01 subg oups o o single agen s and p esen ed
as absolu e consump ion o single classes o as he a io o b oad-
spec um an ibio ics o o al consump ion. An imic obials o he
han an ibio ics (e.g. an imycobac e ials, an ipa asi ics) may also
be a ailable insome cases.
The AWARE index, in oduced by he WHO, appea s o be a
p omising globally o ien ed app oach o da a s a i ica ion and
e alua ion o pe o mance.
53,54
Mos na ional ac ion plans, as well
as he WHO ‘adop AWaRe’ ini ia i e, es ablish goals in e ms o
desi able shi s in consump ion (i.e. educ ion o inc ease in con-
sump ion o speci ic agen s, classes o o he de ined ca ego ies).
Conside ing he in insic need o benchma king and imp o e-
men s in acking, he a ge s p oposed by he expe panel a e
in ended o p omo e alignmen be ween local and e e al AMU
da a. T acking consump ion a he ATC J01 subclass o agen le el
ep esen s he mos desi able op ion, bu i s easibili y is es ic ed
o well-s uc u ed con ex s such as hospi al ou pa ien clinics o
coun ies whe e p ima y ca e se ices a e o ganized on a local
basis and include a cen alized pha macy se ice ha is able o
main ain a comple e and upda edda a low. Consis en wi h o he
human se ings, o he ou pa ien se ing he expe s p oposed a
less demanding, bundle app oach as an essen ial a ge , which
equi es moni o ing, beyond o e all consump ion, o he mos e-
quen ly p esc ibed agen s, including hose in he Wa ch and
Rese e ca ego ies o he WHO AWaRe index and o he an ibio ics
speci ically indica ed by he AMS eam, conside ing local epidemi-
ology (Table3).Thein oduc iono moni o ingo IVan ibio ics
(Table 3, a ge 2.1) inds i s a ionale in he g owing implemen a-
ion o se ices o IV adminis a ion wi hou hospi al s ay h ough
communi y-based managemen , such as ou pa ien pa en e al
an imic obial he apy (OPAT). Fo su eillance pu poses, consump-
ion in he communi y se ing is epo ed as DDDs pe 100 o 1000
inhabi an s. A p e ious consensus e o , aiming o de elop a se
o quan i a i e AMS me ics o be employed in ou pa ien s,
highligh ed he need o combine mo e han one me ic o o e -
come in insic pi alls and op imize in e p e a ion.
39
Conside ing
di e en AMS o ganiza ions and le els o in e en ion, he expe
panel p o ides dis inc s epwise app oaches (Table 3, a ge s 2.4–
2.8). Whe e a cen alized pha macy se ice is in place, DDD-based
me ics a e easy o ob ain and can be ou inely calcula ed o
moni o ing o consump ion, handling cos s and eimbu semen s;
in his con ex , ob aining he numbe o p esc ip ions equi es add-
i ional wo k and dedica ed esou ces. When ini ia i es o AMS
Table 4. An imic obial esis ance and an imic obial s ewa dship in he ou pa ien se ing
Which esis an pa hogens should be a ge ed?
3.1. Essen ial
Iden i y and moni o mos p edominan esis ance pa e ns among u ina y ac cul u es.
How should esis ance be moni o ed?
3.2. Desi able
All samples (ob ained inside and ou side he hospi al) should be clea ly ca ego ized in heal hca e-associa ed o communi y-acqui ed samples o
allow o isk s a i ica ion and di ec empi ical he apy in ou pa ien and hospi al se ings.
Wha ime in e al should be used o epo ing an imic obial esis ance su eillance da a?
3.3. Essen ial
P o ide esis ance su eillance da a a leas yea ly, epo ing only da a o which 30 o mo e isola es a e a ailable.
Should he epo be deli e ed o heal hca e p o essionals o he han he an imic obial s ewa dship eam?
3.4. Essen ial
Deli e a epo o p esc ibing uni s, making hem a ailable o p esc ibe s and ca egi e s, bu also o adminis a ion.
3.5. Desi able
Deli e a epo o p esc ibe s wi h a commen a y; conside highligh ing speci ic da a ha migh equi e e-e alua ion o he apeu ic guidelines.
A ie i e al.
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e o s come om small p esc ibing uni s, simple da abases can
eco d he numbe o p esc ip ions o e ime. As a u he s ep, he
panel encou ages da a s a i ica ion based on p esc ibe speciali y,
and sugges s he acking o p esc ip ions (o e all olumes as well
as ela i e consump ion o speci ic an imic obial agen s/classes)
ackling high-p io i y condi ions, such as hose o which an ibio ics
a e o e p esc ibed (e.g. acu e b onchi is, i al pha yngi is) o a e
likely o be ine ec i e due o inc easing esis ance a es [e.g. u in-
a y ac in ec ions (UTIs) and sexually ansmi ed diseases].
Al hough his app oach equi es de ailed eco ding o p esc ibing
indica ions ha is a ely in place, i s implemen a ion would allow
meaning ul benchma king andda a acking imp o emen s.
The da a collec ed should be egula ly dissemina ed o admin-
is a o s and p esc ibe s (Table 3 a ge s 2.9–2.12). The a o emen-
ioned s a i ica ion should be employed o ailo epo s,
which should also conside he speci ic in e en ion o be imple-
men ed and goals o be pu sued. Regional o local, agg ega ed,
popula ion-based da a should be p o ided o inc ease awa eness
o p esc ibe s and adminis a o s ega ding he dis ance om bes
p ac ice and p og ess made o e ime, as well as o p omo e
sha ed e o s wi hin he same a ea and ac oss he con inuum o
ca e (e.g. e e al hospi als and su ounding LTCFs). The impo -
ance o complemen ing da a dissemina ion wi h s uc u ed edu-
ca ional ac i i ies o os e unde s anding and enhancing desi able
p esc ibing p ac ice is u he s essed by he panel.
De ailed da a o single p esc ibing uni s (small p esc ibe
g oups, ambula o y ca e) o indi idual p esc ibe s allow pee
compa isons o pe o mance, an app oach ha has been demon-
s a ed o be highly e ec i e in ou pa ien AMS.
55,56
To p o ide
meaning ul and close- o-p ac ice da a, annual epo ing is sug-
ges ed. Qua e ly agg ega ed da a and co esponding epo ing,
when olume o use is la ge enough o p o ide eliable da a,
has he po en ial o e eal seasonal ends ha wa an u he
in es iga ion o speci ic coun e measu es.
Sel -medica ion and o e - he-coun e dis ibu ion we e also
acknowledged by he membe s o he panel as issues ha can
ha e an impo an impac on AMR, especially (bu no only) in
LMICs whe e policies egula ing he sale o an imic obials, includ-
ing he equi emen o a p esc ip ion o human use, a e no in
place.
57,58
Es ima ing he amoun o his dispensing ou e was
deemed o be o alue. Howe e , conside ing ha local and na-
ional heal hca e au ho i ies a e esponsible o his a he han
single p ac i ione s o a local AMS eam ac ing in small p esc ibing
uni s, a e discussion he a ge was dele ed om he lis and
ou lined as a opic o u u e esea ch (Table 5).
An imic obial esis ance and an imic obial s ewa dship
Wi h ega d o AMR su eillance, e idence on speci ic pa hogens
o be a ge ed in he ou pa ien se ing is limi ed. The majo i y o
guidance documen s sugges he acking o an ibio ic esis ance
ends among ‘common ou pa ien pa hogens’, communi y-
associa ed Clos idioides di icile in ec ions and in ec ion a es wi h
‘mul id ug- esis an o ganisms’ wi hou speci ying which pa ho-
gens.
22,38,47,48
This limi a ion is mainly ela ed o he ac ha , in
Table 5. Resea ch p io i ies
•De elop s anda dized and eliable su eillance de ini ions and ou come da a
Ra ionale
While c i e ia o disc imina e hospi al- om communi y-acqui ed in ec ions exis , mic obiological samples submi ed om ou pa ien se ings
may no e lec he ue o igin o in ec ions. Resis ance a e in he communi y could be o e es ima ed when o e ep esen a ion o samples om
pa ien s wi h speci ic isk ac o s (e.g. exposu e o heal hca e acili ies such as day se ice p ac ices, indwelling de ice ca ie s, ecu en in ec ions,
e c.) occu s. S anda dized de ini ions allowing unambiguous iews o he mos p obable se ing o in ec ion acquisi ion, u he pa ien -based
s a i ica ion c i e ia (e.g. age, gende , speci ic isk ac o ) and he es ablishmen o he minimum numbe o isola es necessa y o p o ide consis -
en da a, would help in collec ing mo e eliable su eillance da a o in o m p esc ibing p ac ice and empi ical he apy.
•App aise and es ablish new s a egies o AMU su eillance in communi y
Ra ionale
As cu en me ics and o ma s o AMU moni o ing we e de eloped o su eillance no di ec ly conside ing AMS goals and s a egy, he mos
e ec i e me hods o an imic obial consump ion da a collec ion in he communi y se ing s ill ha e o be iden i ied, especially in ega d o i s co -
ela ion wi h an imic obial esis ance ends. The easibili y/ eliabili y o poin p e alence su eys (PPSs) o an ibio ic use in he communi y se ing
ha e been poo ly explo ed un il now.
The assessmen o sel -medica ion and o e - he-coun e dispensing a na ional, egional and local le els ( h ough PPSs o o he sui able
me hodologies) would no only p o ide essen ial da a o co ec ly es ima e ac ual an imic obial consump ion, bu would also guide policymake s
in es ablishing an imic obial dispensing egula ions.
•Gene a e e idence o unde s and he ole o accina ion in AMS
Ra ionale
Many AMR egula o y documen s and AMS guidance poin ou accina ion as a p omising s a egy o limi AMR. E en hough he a ional o his en-
do semen appea s clea , limi ed s udies ha e analysed an imic obial consump ion and esis ance end a ia ions as di ec e ec s o accina ion
campaigns o he associa ion be ween accina ion co e age and an imic obial usage and esis ance a e. Mo e e idence is needed on he e ec
o accines on an ibio ic use and esis ance. Solid s a is ical ools and adequa e s udy designs o assess such a link should be e alua ed and
implemen ed.
Linking su eillance wi h AMS in he ou pa ien se ing JAC
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he ou pa ien con ex , mic obiological analysis o a ious speci-
mens o de e mine pa hogens and ela ed suscep ibili ies is o en
imp ac ical. Some e iew documen s ocus on he mos common
in ec ions, such as espi a o y ac in ec ions (RTIs) and UTIs.
Consequen ly, he mos ele an pa hogens a e S ep ococcus
pneumoniae,Haemophilus in luenzae,Mo axella ca a halis,
Mycoplasma pneumoniae and En e obac e iaceae.
47
Acknowledging he di icul ies associa ed wi h sample collec ion,
he panel conside ed ha moni o ing RTI esis ance in ou pa ien s
is no easible, as only a ew samples a e no mally submi ed o
mic obiological analysis. Acco dingly, i was decided o ocus on
synd omes displaying a g ea e bu den o esis ance, sugges ing
ha esis ance be moni o ed only o UTIs (Table 4, a ge 3.1).
Ne e heless, he impo ance o ca ego izing all samples
(ob ained bo h in and ou o hospi al) in heal hca e-associa ed o
communi y-acqui ed se ings o allow isk s a i ica ion and di ec
empi ical he apy in ou pa ien and hospi al se ings was unde -
lined. Fu he s a i ica ions by gende , age and isk ac o s we e
discussed, bu hey we e no included in he inal a ge s due o
lack o easibili y and eliabili y.
On AMR epo ing, he expe panel ag eed on he ac ha he
epo should be deli e ed o all p esc ibing uni s and heal hca e
au ho i ies. I should be made a ailable o adminis a ion, p e-
sc ibe s, ca egi e s and nu ses o all uni s. The expe panel u he
s essed he impo ance no only o passi ely deli e ing a epo ,
bu also o linking dissemina ion o su eillance da a wi h s uc-
u ed educa ional ac i i ies o imp o e unde s anding and d i e
clinical p ac ice. Howe e , conside ing possible esou ce con-
s ain s, his was held o be desi able and no essen ial ( a ge 3.5).
I was also sugges ed ha an English e sion o he epo be
included o os e he sha ing o in o ma ion be ween coun ies.
Mo eo e , as p e iously ad oca ed,
58
he panel highligh ed he
ac ha educa ional e o s should a ge no only physicians, bu
also unde g adua e s uden s. In his con ex , he unde g adua e
cu iculum could be expanded o allow eaching o he p inciples
o mic obiology, in ec ious diseases and clinical pha macology
wi h emphasis on AMR and p uden p esc ibing.
The a ailable li e a u e did no allow he de elopmen o
de ailed indica ions on a ew impo an ques ions ela ed o AMU
epo ing and AMR moni o ing and epo ing in he ou pa ien se -
ing. The esea ch ques ion ini ially o mula ed o opic 2, ‘Which
c i e ia should be used o de ine a anking o an ibio ic use?’, and
he esea ch ques ions o opic 3, ‘Should non-clinical samples (e.g.
sc eening) be moni o ed?’, ‘Should speci ic h esholds be es ab-
lished o d i ing AMS ecommenda ions o empi ical he apy?’
and‘Which s a i ica ion should be used o d i eselec i e epo ing
o an ibiog ams?’, should he e o e be conside ed p io i ies o u-
u e esea ch. Th ee main esea ch p io i ies including inpu s o
policymake s a e summa ized in Table5. Las ly, he panel dis-
cussed he impo ance o expanding a simila lis o consensus a -
ge s o ube culosis and o he pa hogens ( ungi and i uses) in
he u u e.
Conclusions
The 22 a ge s de eloped he ein we e concep ualized as a lis o
p agma ic and b oadly applicable ac ions o guide de elopmen o
an AMS p og amme in he ou pa ien se ing. Despi e he in insic
limi a ions gi en by he subjec i e na u e o expe opinion
me hodology, one s eng h o his wo k is ha he a ge ac ions
ha e been p oposed by a b oad panel o p o essionals, encom-
passing human and e e ina y medicine in a One Heal h app oach.
Ano he s eng h o his wo k is he ca ego iza ion o he a ge
ac ions as essen ial (conside ed as he minimum equi emen s)
and desi able (ac ions o be conside ed o he u he and op imal
implemen a ion o an AMS plan), aking in o accoun low- esou ce
se ings, including hose cha ac e ized by lack o quali ied pe son-
nel and labo a o y in as uc u e due o budge cons ain s.
Acknowledgemen s
We a e e y g a e ul o Ru h Joanna Da is o he suppo in he man-
agemen o he p ojec , and o Michaela Ha diman and Nadine
Conzelmann o hei adminis a i e suppo .
Membe s o he ARCH wo king g oup
Ayola Akim Adegnika, Cen e de Reche ches Me´dicales de Lamba e´ne´
(CERMEL), Lamba e´ne´, Gabon, and Ins i u u¨ T openmedizin and
Ge man Cen e o In ec ion Resea ch, pa ne si e Tu¨bingen,
Uni e si a¨ sklinikum, Wilhelms aße, Tu¨bingen, Ge many; Fabiana A ie i,
In ec ious Diseases Sec ion, Depa men o Diagnos ics and Public
Heal h, Uni e si y o Ve ona, Ve ona, I aly; Ni hya Babu Rajend an,
In ec ious Diseases, Depa men o In e nal Medicine I, Tu¨bingen
Uni e si y Hospi al, Tu¨bingen, Ge many, and Ge man Cen e o In ec ion
Resea ch (DZIF), Clinical Resea ch Uni o heal hca e associa ed in ec-
ions, Tu¨bingen, Ge many; Julia Bielicki, Pedia ic In ec ious Diseases,
Uni e si y Child en’s Hospi al Basel, Basel, Swi ze land, and Pedia ic
In ec ious Disease Resea ch G oup, Ins i u e o In ec ion and Immuni y,
S Geo ge’s Uni e si y o London, London, UK; S e en Bo mann, Cen e
de Reche ches Me´dicales de Lamba e´ne´ (CERMEL), Lamba e´ne´, Gabon,
and Ins i u u¨ T openmedizin and Ge man Cen e o In ec ion
Resea ch, pa ne si e Tu¨bingen, Uni e si a¨ sklinikum, Wilhelms aße,
Tu¨bingen, Ge many; Elena Ca a a, In ec ious Diseases Sec ion,
Depa men o Diagnos ics and Public Heal h, Uni e si y o Ve ona,
Ve ona, I aly; Robe o Cauda, Ins i u e o In ec ious Diseases,
Fondazione Policlinico Uni e si a io A. Gemelli IRCCS, Uni e si a` Ca olica
del Sac o Cuo e, Rome, I aly; Monica Comp i, In ec ious Diseases Sec ion,
Depa men o Diagnos ics and Public Heal h, Uni e si y o Ve ona,
Ve ona, I aly; Giulia De Angelis, Dipa imen o di Scienze Bio ecnologiche
di base, Cliniche In ensi ologiche e Pe iope a o ie, Uni e si a` Ca olica
del Sac o Cuo e, Rome, I aly; Raquel Du o, Uni o he P e en ion and
Con ol o In ec ion and An imic obial Resis ance, Cen o Hospi ala
Uni e si a´ io de S~
ao Jo~
ao, Opo o, Po ugal; Isabel F os , Cen e o
Disease Dynamics, Economics & Policy, New Delhi, India; Facul y o
Medicine, Depa men o In ec ious Disease, Impe ial College, London,
UK; Liliana Galia, In ec ious Diseases Sec ion, Depa men o Diagnos ics
and Public Heal h, Uni e si y o Ve ona, Ve ona, I aly; Pe a Gas meie ,
Ge man Cen e o In ec ion Resea ch Associa ion (DZIF), B aunschweig,
Ge many, and Ins i u e o Hygiene and En i onmen al Medicine, Cha i e´
- Uni e si a¨ smedizin Be lin, Ge many, co po a e membe o F eie
Uni e si a¨ Be lin, Humbold -Uni e si a¨ zu Be lin, and Be lin Ins i u e o
Heal h; Ch is ian Giske, Depa men o Clinical Mic obiology, Ka olinska
Uni e si y Hospi al, S ockholm, Sweden; Depa men o Labo a o y
Medicine, Ka olinska Uni e si y Hospi al, S ockholm, Sweden; Si i Go¨pel,
In ec ious Diseases, Depa men o In e nal Medicine I, Tu¨bingen
Uni e si y Hospi al, Tu¨bingen, Ge many, and Ge man Cen e o In ec ion
Resea ch (DZIF), Clinical Resea ch Uni o heal hca e associa ed in ec-
ions, Tu¨bingen, Ge many; He man Goossens, Depa men o Medical
Mic obiology, Vaccine & In ec ious Disease Ins i u e, Uni e si y o
An we p, An we p, Belgium; Gunna Kahlme e , Depa men o Clinical
Mic obiology, Va¨xjo¨ Cen al Hospi al, Va¨xjo¨, Sweden; Souha S. Kanj,
A ie i e al.
ii48
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Di ision o In ec ious Diseases, Depa men o In e nal medicine, and
In ec ion Con ol and P e en ion P og am, and An imic obial
S ewa dship P og am, Ame ican Uni e si y o Bei u Medical Cen e ,
Bei u , Lebanon; Tomisla Kos yane , Depa men o Medical
Mic obiology, Vaccine & In ec ious Disease Ins i u e, Uni e si y o
An we p, An we p, Belgium; Leona d Leibo ici, Medicine E, Rabin Medical
Cen e , Beilinson Hospi al, Pe ah Tik a, Is ael, and Facul y o Medicine,
Tel-A i Uni e si y, Tel-A i , Is ael; Jean-Ch is ophe Luce , In ec ion
Con ol Uni , Bicha -Claude Be na d Hospi al, AP-HP, Pa is, F ance; IAME,
UMR 1137, DeSCID eam, Uni e si e´ Pa is Dide o , So bonne Pa is Ci e´,
Pa is, F ance; Lo ena Lo´pez-Ce e o, Mic obiology and In ec ious Diseases
Uni , Uni e si y Hospi al Vi gen Maca ena, Se illa, Spain; Rodolphe
Made , Uni e si y o Lyon, F ench Agency o Food, En i onmen al and
Occupa ional Heal h and Sa e y (ANSES), Labo a o y o Lyon,
An imic obial Resis ance and Bac e ial Vi ulence Uni , Lyon, F ance;
Ful ia Mazza e i, In ec ious Diseases Sec ion, Depa men o Diagnos ics
and Public Heal h, Uni e si y o Ve ona, Ve ona, I aly; Elena Mazzolini,
Depa men o Epidemiology, Is i u o Zoop o ila ico Spe imen ale delle
Venezie, Legna o, Padua, I aly; Ma c Mendelson, Di ision o In ec ious
Diseases and HIV Medicine, Depa men o Medicine, Uni e si y o Cape
Town, Cape Town, Sou h A ica; Ri a Mu i, Ins i u e o In ec ious
Diseases, Fondazione Policlinico Uni e si a io A. Gemelli IRCCS, Uni e si a`
Ca olica del Sac o Cuo e, Rome, I aly; Nico T. Mu e s, Ins i u e o
Hygiene and Public Heal h, Bonn Uni e si y Hospi al, Bonn, Ge many;
Mical Paul, Diseases Ins i u e, Rambam Heal h Ca e Campus, Ru h and
B uce Rappapo Facul y o Medicine, Technion - Is ael Ins i u e o
Technology, Hai a, Is ael; Ma ia Dile a Pezzani, In ec ious Diseases
Sec ion, Depa men o Diagnos ics and Public Heal h, Uni e si y o
Ve ona, Ve ona, I aly; Elisabe h P es e l, Eu opean Commi ee on
In ec ion Con ol, Basel, Swi ze land, and Depa men o In ec ion
Con ol and Hospi al Epidemiology, Medical Uni e si y o Vienna, Vienna,
Aus ia; Hanna Renk, Uni e si y Child en’s Hospi al Tu¨bingen,
Depa men o Paedia ic Ca diology, Pulmology and In ensi e Ca e
Medicine, Tu¨bingen, Ge many; Oana Sandulescu, Depa men o
In ec ious Diseases I, Facul y o Medicine, Ca ol Da ila Uni e si y o
Medicine and Pha macy, Bucha es , Na ional Ins i u e o In ec ious
Diseases ‘P o . D Ma ei Bals¸’ Bucha es , Romania; Le Huu Song,
Vie namese Ge man Cen e o Medical Resea ch, Hanoi, Vie nam, and
108 Mili a y Cen al Hospi al, Hanoi, Vie nam; Mau izio Sanguine i,
Dipa imen o di Scienze Bio ecnologiche di base, Cliniche
In ensi ologiche e Pe iope a o ie, Uni e si a` Ca olica del Sac o Cuo e,
Rome, I aly, and Dipa imen o di Scienze di Labo a o io e
In e i ologiche, Fondazione Policlinico Uni e si a io A. Gemelli IRCCS,
Rome, I aly; Remco Sch ij e , Ve E ecT, Bil ho en, The Ne he lands;
Luigia Scudelle , Scien i ic Di ec ion o IRCCS Ca’ G anda Ospedale
Maggio e Policlinico di Milano, Milano, I aly; Mike Sha land, Paedia ic
In ec ious Diseases Resea ch G oup, Ins i u e o In ec ion and
Immuni y, S Geo ge’s Uni e si y o London, London, UK; Ma cella Sibani,
In ec ious Diseases Sec ion, Depa men o Diagnos ics and Public
Heal h, Uni e si y o Ve ona, Ve ona, I aly; E elina Tacconelli, In ec ious
Diseases Sec ion, Depa men o Diagnos ics and Public Heal h,
Uni e si y o Ve ona, Ve ona, I aly, and In ec ious Diseases, Depa men
o In e nal Medicine I, Tu¨bingen Uni e si y Hospi al, Tu¨bingen, Ge many,
and Ge man Cen e o In ec ion Resea ch (DZIF), Clinical Resea ch Uni
o heal hca e associa ed in ec ions, Tu¨bingen, Ge many; Didem
To umkuney, In e na ional Fede a ion o Pha maceu ical Manu ac u e s
and Associa ions (IFPMA), Gene a, Swi ze land; Thi umalaisamy P.
Vela an, Ins i u e o T opical Medicine, Uni e si a¨ sklinikum Tu¨bingen,
Ge many, and Vie namese Ge man Cen e o Medical Resea ch, Hanoi,
Vie nam, and Facul y o Medicine, Duy Tan Uni e si y, Da Nang, Vie nam;
And eas Voss, Depa men o Medical Mic obiology, Radboud Uni e si y
Medical Cen e, Nijmegen, The Ne he lands.
Funding
This esea ch p ojec has ecei ed unding om he Inno a i e
Medicines Ini ia i e Join Unde aking unde g an ag eemen No.
115737, esou ces o which a e composed o inancial con ibu ion om
he Eu opean Union Se en h F amewo k P og amme (FP7/2007-2013)
and Eu opean Fede a ion o Pha maceu ical Indus ies and Associa ions
(EFPIA) companies in-kind con ibu ion, and he Ge man Fede al Minis y
o Educa ion and Resea ch (BMBF) (P ojec ID 01KI1830) unde he Join
P og amme Ini ia i e on An imic obial Resis ance (JPIAMR) 2018 call.
T anspa ency decla a ions
The au ho s ha e none o decla e. Pa ick Moo e o Ad ia ic Heal h
Communica ions p o ided medical w i ing se ices o he edi ing and
p oo ing o his pape . This a icle o ms pa o a Supplemen .
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