Whi e Pape : B idging he gap be ween su eillance da a and
an imic obial s ewa dship in he animal sec o —p ac ical guidance
om he JPIAMR ARCH and COMBACTE-MAGNET EPI-Ne ne wo ks
Monica Comp i
1
†, Rodolphe Made
2
*†, Elena Mazzolini
3
†, Giulia de Angelis
4,5
, Nico T. Mu e s
6
,
Ni hya Babu Rajend an
7,8
, Liliana Galia
1
, E elina Tacconelli
1,7,8
and Remco Sch ij e
9
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
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;
3
Depa men o Epidemiology, Is i u o Zoop o ila ico Spe imen ale delle Venezie, Legna o,
Padua, I aly;
4
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;
5
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;
6
Ins i u e o Hygiene and Public Heal h, Bonn Uni e si y Hospi al, Bonn, Ge many;
7
In ec ious Diseases, Depa men o
In e nal Medicine I, Tu¨bingen Uni e si y Hospi al, Tu¨bingen, Ge many;
8
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;
9
Ve E ecT, Bil ho en, The Ne he lands
*Co esponding au ho . E-mail: odolphe.made @anses.
†Equally con ibu ing i s au ho s.
‡Membe s a e lis ed in he Acknowledgemen s sec ion.
Backg ound: The JPIAMR ARCH and COMBACTE-MAGNET EPI-Ne ne wo ks ha e joined e o s o o mula e a se
o a ge ac ions o link he su eillance o an imic obial usage (AMU) and an imic obial esis ance (AMR) wi h
an imic obial s ewa dship (AMS) ac i i ies in ou di e en se ings. This Whi e Pape ocuses on he e e ina y
se ing and emb aces he One Heal h app oach.
Me hods: A e iew o he li e a u e was ca ied ou add essing esea ch ques ions in h ee a eas: AMS leade ship
and accoun abili y; AMU su eillance and AMS; and AMR su eillance and AMS. Consensus on a ge 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 o-
biology, AMS, e e ina y medicine and public heal h, om 18 coun ies.
Resul s/discussion: Fo y-six a ge ac ions we e de eloped and quali ied as essen ial o desi able. Essen ial
ac ions included he se up o AMS eams in all e e ina y se ings, building go e nmen -suppo ed AMS p o-
g ammes and ollowing speci ic equi emen s on he p oduc ion, collec ion and communica ion o AMU and
AMR da a. Ac i i ies o AMS eams should be ailo ed o he local si ua ion and capaci ies, and be linked o local
o na ional su eillance sys ems and in ec ion con ol p og ammes. Se e al esea ch p io i ies we e also iden i-
ied, such as he need o de elop mo e clinical b eakpoin s in e e ina y medicine.
Conclusions: This Whi e Pape o e s a p ac ical ool o e e ina y p ac i ione s and policy make s o imp o e
AMS in he One Heal h app oach, hanks o su eillance da a gene a ed in he e e ina y se ing. This wo k may
also be use ul o medical doc o s wishing o be e unde s and he speci ici ies o he e e ina y se ing and a-
cili a e c oss-sec o al collabo a ions.
In oduc ion
Ve e ina y and human medicine sha e he esponsibili y o p e-
se ing he e icacy o an ibio ics and p e en ing he sp ead o
an imic obial esis ance (AMR). To a la ge ex en , he an imic obial
d ugs (o classes) ha a e used in animals a e he same as hose
in human se ings
1–3
and esis an bac e ia can be ans e ed
be ween animals, he en i onmen and humans h ough di e en
ou es o ansmission.
1–4
This ende s AMR a One Heal h issue
equi ing mul i-sec o al collabo a ions.
4–6
To p e en he sp ead o AMR, an imic obial s ewa dship (AMS)
should be de eloped collec i ely in all se ings whe e an imic o-
bials a e used as ‘a cohe en se o ac ions which p omo e using
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]
ii52
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an imic obials esponsibly’.
7
Indeed, AMS in e en ions in one se -
ing can ha e a posi i e impac in ano he ,
5
and his is pa icula ly
he case o he animal sec o , whe e in e en ions a e commonly
ca ied ou wi h a public heal h pe spec i e.
1,8,9
Howe e , he
speci ici ies o each se ing should always be ca e ully aken in o
accoun when de ising an AMS p og amme.
10–14
The e e ina y sec o is highly he e ogeneous. Ve e ina ians
can wo k as independen p i a e p ac i ione s (ac ing alone) o be
o ganized in e e ina y clinics o hospi als wi h mul iple s a , ha
can be owned by indi iduals o by na ional o mul ina ional e e -
ina y heal hca e en e p ises. Ve e ina ians deal wi h di e en ani-
mal species ha include companion animals, ood-p oducing
animals and, al hough less commonly, wild animals. Ve e ina ians
can p esc ibe and dispense an imic obials o a ious pu poses, i.e.
ea men , me aphylaxis (adminis a ion o a d ug o a g oup
o clinically heal hy animals in con ac wi h diseased animals),
15
p e en ion and g ow h p omo ion (whe e allowed) o indi idual
animals o g oups o animals.
15–17
Access o an imic obials also
di e s g ea ly be ween coun ies
18–20
and is some imes eadily
a ailable wi hou any p esc ip ion o a me s o pe owne s,
21–23
leading o u he di icul ies in con olling an imic obial usage
(AMU).
Moni o ing AMU is impo an o quan i a i ely assess he pe -
o mance o a Na ional Ac ion Plan (NAP) in educing he o e all
use o an imic obials, o a ge in e en ions in animal species o
p e en using unjus i ied amoun s o an imic obials and o check
ha he e e ina y use o an imic obials c i ically impo an o
human heal h is minimized.
24–26
When ca ied ou a he le el o
p esc ip ion, i can become a benchma king ool whe e p esc ibe s,
selle s o a me s can compa e hei an imic obial usage agains a
egional a e age o a pa icula ood-p oduc ion sec o .
27–30
Al hough such sys ems may equi e speci ic legisla ion, hey can
be use ul o educe AMU, especially when linked wi h incen i es o
lowe usage o a ge ed in e en ions o high an imic obial
use s.
31
I is no ewo hy ha NAPs on AMR, al hough ecom-
mended by he Wo ld Heal h O ganiza ion (WHO) and WHO
Membe S a es, a e no legally binding. This limi s he powe o
NAPs as a go e nance ool.
32
In addi ion, i is key o moni o AMR in animal bac e ial pa ho-
gens
33–35
o help e e ina ians and a me s use an imic obials
mo e p uden ly, ollow AMR ends and ad ise ac ion a na ional o
mo e local le els. Mo eo e , showing AMS eams and o he ac o s
in animal heal h ha hei e o s succeed no only in dec easing
AMU bu also AMR is necessa y o main ain hei commi men . In
he One Heal h app oach i is also pa amoun o moni o AMR in
zoono ic and commensal bac e ia
36,37
om heal hy animals o as-
sess he isk o ansmission o humans h ough he ood chain (o
by di ec con ac ), as his can lead o be e isk managemen
in e en ions.
38
O no e, commensal bac e ia a e a use ul indica o
o he compa ison o AMR a es o e ime and be ween di e en
animal species, coun ies o a ms.
Despi e a gene al call o de elop moni o ing sys ems ha a e
able o p o ide ele an , accu a e and comple e da a o d i e AMS
p og ammes in all se ings, including he animal sec o , many
gaps s ill emain, along wi h many ha moniza ion challenges.
Fo example, only agmen a y da a on AMU and AMR a e a ailable
o companion and aqua ic animals.
39–42
Rega ding AMR da a,
mos o he a ailable in o ma ion comes om heal hy e es ial
ood-p oducing animals and ela i ely ew mul i-annual
p og ammes a e in place o he moni o ing o AMR in animal
pa hogens.
43–45
The complexi y o he e e ina y se ing (including i s in e -
connec ions wi h he human sec o , he a ying pu poses o
su eillance sys ems
26,46,47
and he non-homogeneous a ailabili y
o su eillance da a and esou ces a ound he wo ld
48,49
) make
many ac i i ies di icul o s anda dize. Thus, p ac ical de ails
a e no a ailable o many AMS ac i i ies, and indica ions on how
su eillance da a should in e wine wi h AMS in e en ions a e
lacking.
The JPIAMR ARCH
50
and COMBACTE-MAGNET EPI-Ne
51
ne -
wo ks ha e come oge he o he sha ed goal o implemen ing a
amewo k o ac ions o acili a e an ibio ic policy in e en ions
and os e use o su eillance da a on AMR and consump ion and
implemen a ion o AMS ac i i ies inhuman and animal heal h.
In his ega d, he ARCH and COMBACTE-MAGNET EPI-Ne
in e na ional expe panel is ocusing on ou se ings: hospi al,
ou pa ien , long- e m ca e acili y, and e e ina y. The e o s in-
ol e h ee a eas: (i) AMS leade ship and accoun abili y; (ii) AMU
and AMS; and (iii) AMR and AMS, all conside ing he easibili y o
he ac ions and he One Heal h app oach.
This Whi e Pape ocuses on he e e ina y sec o and a ge s
e e ina ians, policymake s and o he ac o s in animal and human
heal h who a e in ol ed in AMS ac i i ies. The p oposed guidance
is in ended as a p ac ical ool ega ding he p oduc ion and use o
AMU and AMR da a o plan and implemen AMS p og ammes
in line wi h he One Heal h app oach and applicable in di e en
e e ina y con ex s, including esou ce-limi ed coun ies.
Dissemina ion o he in ended audience will be ensu edby he ne -
wo ks in ol ed in he JPIAMR ARCH p ojec as lis ed in Table 1o
he i s pape in his se ies.
52
Checklis o ma s o he a ge
ac ions a e downloadable om he ARCH websi e.
50
These check-
lis s can be used by heal h p o essionals and policymake s o
es ablish and/o moni o s ewa dship ac i i ies.
Me hods
Adop ing a One Heal h app oach, he p esen p ojec was planned o de-
elop expe consensus conside ing he li e a u e and guidance on AMS
and su eillance. A i s d a o a ge s and a RAND-modi ied Delphi p o-
cess we e used o alida ion o a ge s (p o ocol on ARCH websi e).
50
The p ocess in ol ed de elopmen o key esea ch ques ions a ising
om a sys ema ic e iew on su eillance epo ing o AMR ha was
p e iously de eloped (EPI-Ne COACH p ojec )
53
and adap ed o a e e -
ina y se ing (Table 1); a na a i e e iew o he a ailable e idence was
pe o med, and a i s d a o a ge s was p o ided o he expe s in a
web-based su ey. Ag eemen was exp essed on a nine-poin Like
scale. A 2 day ace- o- ace mee ing ook place a he end o Oc obe
2019. A li e a u e sea ch o ele an publica ions in English, published in
he las 10 yea s, was ca ied ou using MEDLINE (Na ional Lib a y o
Medicine, Be hesda, MD, USA) using a combina ion o he ollowing
e ms: an imic obial*, consump ion, animal*, e e ina y, an imic obial
d ug esis ance, su eillance. Mo e de ails a e a ailable in he i s pape
in his se ies.
52
Du ing he mee ing, he expe s we e p esen ed wi h a summa y o
he a ailable e idence and he esul s o he online su ey. The en i e se o
a ge s was e iewed and discussed. Following he mee ing, a co e eam
(M.C., E.M., R.M., R.S.) o he e e ina y wo king g oup pe o med a u he
e ision and ine- uning o he lis o a ge s, which was hen app o ed by
he en i e panel in an addi ional consul a ion. To co e all di e en e e in-
a y ea u es and ela ed in e connec ions wi h human heal h, di e en
An imic obial su eillance and s ewa dship in he animal sec o JAC
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se ings ( a ms, e e ina y clinics, e c.) and animal popula ions (companion
and ood-p oducing animals, including aqua ic animals) we e conside ed.
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 e e ina y 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 p ac icable i
no al eady b oadly accomplished, and ‘desi able’ in he case o limi ed
easibili y o ha ing a esou ce-in ensi e na u e. Topics o which mo e
e idence was equi ed in o de o d aw up ecommenda ions we e added
as p io i y opics o u he esea ch.
O e 40 expe s om 18 coun ies and ep esen ing 30 ne wo ks de el-
oped 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).
52
Resul s
A o al o 49 guidance documen s (23 in e na ional and 26 na ion-
al documen s) and 45 a icles including sys ema ic e iews, s ud-
ies and expe opinions we e included o he ull e idence
app aisal.
1,3,4,8–17,19,20,22,24,27,28,31,33,34,36–38,40,41,46–48,54–117
In e -
na ional and na ional guidelines, p ac ical guides o ools,
su eillance epo s and sys ema ic e iews p o ided mos o
he e idence. The majo i y o he documen s (71/94, 76%) we e
om high-income coun ies (Eu ope, No h Ame ica, Aus alia
and New Zealand).
Fo wo esea ch ques ions (‘Should he epo se speci ic
h esholds o es ablishing empi ical he apy and su gical p ophy-
laxis?’ and ‘Which c i e ia should be used o d i e selec i e epo -
ing o an ibiog ams?’), he in o ma ion did no allow d a ing o
speci ic a ge s, and hus hese opics we e add essed as u u e
esea ch a eas.
An ini ial se o 65 a ge s was de eloped based on e ie ed
documen s and assessed by eigh expe s in he ield o human
and e e ina y medicine h ough he online su ey. Consensus
was eached on 54 a ge s, and addi ional commen s we e p o-
ided o mos o hem.
Ele en a ge s, whe e he ag eemen was no eached a e
i s consul a ion, we e discussed in he mee ing. Main opics o
discussion e ol ed a ound: (i) he o ganiza ion o AMS conside ing
pa icipan s and oles o he AMS eam and ins i u ional suppo ;
(ii) bac e ial species o moni o conside ing human and animal
heal h; and (iii) how o deal wi h he lack o clinical b eakpoin s o
implemen AMS ac i i ies. Nine a ge s we e dele ed du ing he
mee ing. All o he a ge s we e econside ed and p oposed o
eph asing (some we e me ged o spli ) o addi ional e alua ion
ollowing he sugges ions o he panel.
A e he mee ing, a lis o 46 e ised a ge s (25 essen ial and
21 desi able) was d a ed by he co e g oup and app o ed by he
en i e expe panel. Tables2–4, espec i ely, lis he ecommended
a ge s o AMS leade ship and accoun abili y, AMU and AMS, and
AMR and AMS. Tables 5–8 e e o he s a emen s o Tables 2–4.
Discussion
In e es ingly, AMS leade ship and accoun abili y in he animal sec-
o was one o he main opics o discussion du ing he mee ing.
This may e eal ha mo e e o s ha e been made o de elop AMR
and AMU su eillance sys ems in compa ison wi h e o s o s uc-
u ing and guiding AMS ac i i ies in e e ina y p ac ices. Al hough
p elimina y ag eemen was eached o all p oposed a ge s bu
one wi hin he online su ey, commen s and sugges ions we e
p o ided du ing he consul a ions ha equi ed u he e alua ion.
This is likely due o he b oad he e ogenei y o he e e ina y sec o
conside ing animal species, animal popula ions ( ood-p oducing
animals including aquacul u e and companion animals) and he
a ious con ex s whe e animal heal hca e is p o ided ( a ms,
small e e ina y clinics, la ge hospi als, e c.).
The expe g oup is awa e ha he desi able composi ion o he
AMS eam desc ibed is o en no easible, bu he ac ion poin aims
o de ine he bes op ions when es ablishing an AMS eam. Ve y
o en, he eam may be composed o only a a me and his/he
e e ina ian, wo king oge he o a ionalize AMU. Howe e , o
la ge clinics and a ming indus ies ha ha e hei own pha ma-
cies and labo a o ies, he composi ion o he AMS eam could
come close o wha is ecommended.
10,12,54,99,100
Deba es also a ose ega ding he ole o animal owne s.
Al hough pe owne s a e esponsible o he adminis a iono an i-
mic obial ea men s o hei animals, i is no ealis ic o include
hem in AMS eams. On he o he hand, a me s (and also b eede s
o ho ses o companion animals), who a e p o essional animal
keepe s, do bea esponsibili y o he p uden use o an ibio -
ics
11,55,56
and ha e a majo ole o play in AMS.
4,19,90
S ill, pe own-
e s should be a ge ed by educa ional ac i i ies o os e he
Table 1. Key ques ions o he e e ina y se ing
1. Leade ship commi men , accoun abili y and an imic obial s ewa d-
ship eam
- Pa icipan s in he an imic obial s ewa dship eam
- Ta ge s o an imic obial s ewa dship (e.g. is an imic obial s ewa dship
a ge ed o diseased animals?)
- Ins i u ional suppo o o ganiza ion and managemen o
an imic obial s ewa dship p og ammes: legal amewo k
- Ins i u ional suppo o o ganiza ion and managemen o
an imic obial s ewa dship p og ammes: s a ing pe sonnel
2. An imic obial usage and an imic obial s ewa dship
- Which an ibio ics should be moni o ed?
- Which me ics should be employed o moni o ing an imic obial usage?
- Should he su eillance speci y he pu pose o an imic obial usage?
- Which c i e ia o epo ing and ime in e al should be used?
- Who should be he end use o he epo ?
- Should a es ic i e policy be adop ed?
- Should a anking o an ibio ic use be adop ed?
3. An imic obial esis ance and an imic obial s ewa dship
- Which c i e ia a e needed o a ge esis an pa hogens?
- How should esis ance be moni o ed?
- Which p e alence da a and selec i e moni o ing sc eening should be
conside ed?
- Which c i e ia o epo ing and ime in e al should be used?
- Which c i e ia should be applied o s a i y he esul s?
- Who should be he end use o he epo ?
- Should he epo se speci ic h esholds o es ablishing empi ical
he apy and su gical p ophylaxis?
- Which c i e ia should be used o d i e selec i e epo ing o
an ibiog ams?
Comp i e al.
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app op ia e use o an imic obials, along wi h e e ina ians,
a me s and o he ac o s in animal heal h.
13,58,101,118
AMS should be implemen ed om he local o he global
le el, spanning human heal h, animal heal h and he en i on-
men .
2,12,58,119
The e o e, e en in he e e ina y se ing, AMS
should be de ised and suppo ed a a highe le el, especially by
go e nmen s and indus y
57,59,60,110
in he o m o NAPs and good
p ac ice cha e s. These should ecommend measu es o educe
AMR and p o ide guidance o AMS eams in he ield. Se ing
a ge s o educ ion,
61,62
as well as es ic ing AMU in ani-
mals,
9,41,63,104
has been shown o be e y e ec i e in se e al coun-
ies.
120
To os e AMS, go e nmen s should suppo AMU and AMR
moni o ing sys ems.
39,58,59,113
Mo e b oadly, ins i u ional suppo
is c ucial in e ms o communica ion and p og ess epo ing, and
o ensu e anspa ency o in o ma ion on bo h AMU and AMR.
The e mus also be suppo o any olun a y app oaches,
p o ided hey a e in line wi h go e nmen policy.
60
Fo example,
indus y ini ia i es o es ic he use o some an imic obial classes
ha e been shown o be e icien a educing esis ance a es
120,121
and should be encou aged. The de elopmen o quali y policies in
e e ina y clinics wi h a dedica ed componen on AMS ac i i ies
should also be p omo ed.
The design o AMU o AMR moni o ing sys ems should depend
on hei objec i es, exis ing con ex s and capaci ies, and be
consis en wi h na ional guidelines, i any.
14,48
Howe e , exis ing
policies on access and use o an imic obials may di e subs an ial-
ly among coun ies.
19,21,22,42,56
A e e ina y p esc ip ion may o
may no be compulso y, impai ing he a ailabili y o he d-le el
benchma king. Addi ionally, he lack o na ional legisla ions/ egu-
la ions s ill pe mi s some coun ies o use an imic obials as g ow h
p omo e s,
17,18,122
al hough his p ac ice is s ongly discou aged
by in e na ional o ganiza ions, including he WHO,
1
he Wo ld
O ganisa ion o Animal Heal h (OIE),
123
and Eu opean legisla-
ion.
15
To help in hei design, ankings o an imic obials om in e -
na ional o ganiza ions can be used (WHO, OIE, EMA), in pa icula
ca ego iza ions ha conside he isk ha animal usage o an imi-
c obials may pose o public heal h in he One Heal h app oach.
9
The consensus be ween expe s ega ding AMU s a emen s
was easily achie ed, likely due o he nume ous e o s ha ha e
al eady been es ablished in his ield, namely in he amewo k o
he Eu opean Su eillance o Ve e ina y An imic obial
Consump ion (ESVAC). I usage o all an imic obials canno be
moni o ed, as would be desi able,
64
a ge ing speci ic animal
species and an imic obial classes is p e e ed. A majo issue is
ha AMU da a can be collec ed in di e en ways.
26,28,40,92
When
possible, p esc ip ions and, e en be e , animal adminis a ion
da a should be collec ed om e e ina ians and a me s as hese
p o ide he mos accu a e da a on AMU (when p ope ly eco ded)
and allow benchma king.
27,36,62,112
I his is no possible, sales
da a may be collec ed om pha maceu ical companies.
26,65,66
Table 2. Leade ship commi men , accoun abili y and an imic obial s ewa dship eam
An imic obial s ewa dship p og amme and eam
1.1. Essen ial
An imic obial s ewa dship p og ammes should be in place in e e y se ing whe e an imic obials a e used o ea ood-p oducing o companion ani-
mals, wi h a ge s and in e en ions ailo ed o he local si ua ion and linked o local and na ional su eillance sys ems and in ec ion con ol
p og ammes.
1.2. Essen ial
An imic obial s ewa dship p og ammes should be de ined, planned, implemen ed and e alua ed by a dedica ed and compe en eam. This eam
should be ailo ed, depending on he animal species and p oduc ion ype, o he local con ex and a ailabili y o esou ces and pe sonnel.
1.3. Desi able
The eam should include a e e ina ian compe en in an imic obial s ewa dship and ep esen a i es o all p o essionals in ol ed in animal ca e
(pa a- e e ina ians, e e ina y nu ses, a me s, e e ina y pha macis s, mic obiologis s om diagnos ic labo a o ies, e c.) in a collabo a i e ap-
p oach, unde he leade ship o he e e ina ian. This eam should seek p o essional ad ice om addi ional expe s when needed o adequa ely
ul il hei an imic obial s ewa dship ac i i ies.
Ins i u ional suppo o o ganiza ion and managemen o an imic obial s ewa dship p og ammes
1.4. Essen ial
An imic obial s ewa dship p og ammes should be suppo ed a he go e nmen al le el h ough amewo ks such as he Na ional Ac ion Plan in line
wi h ele an in e na ional s anda ds. The Na ional Ac ion Plan should include egula o y decisions o es ic he usage o an imic obials in ood-
p oducing and companion animals, se speci ic educ ion a ge s o an imic obial usage and es ablish moni o ing sys ems o an imic obial usage
and an imic obial esis ance.
1.5. Desi able
Su eillance da a on an imic obial usage and an imic obial esis ance should be made eely a ailable o local an imic obial s ewa dship eams, as
well as o all o he p o essionals wo king in animal, human o en i onmen al heal h.
1.6. Desi able
Volun a y app oaches o imp o e an imic obial s ewa dship and su eillance in he animal sec o should be encou aged, e.g. when he a ming in-
dus y adop s i s own measu es o inc ease biosecu i y, in ec ion con ol and educe an imic obial usage.
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Table 3. An imic obial usage and an imic obial s ewa dship
Which ypes o an imic obial usage, animal species and an imic obials should be moni o ed?
2.1. Essen ial
An imic obial usage should be moni o ed wha e e he pu pose o an imic obial adminis a ion. This includes g ow h p omo ion, a p ac ice ha should be discou aged.
2.2. Essen ial
An imic obial usage should be moni o ed in ood-p oducing (including aqua ic) and companion animals.
2.3. Desi able
An imic obial usage should be moni o ed o all animals o which an imic obials a e au ho ized in a coun y.
2.4. Essen ial
I na ional moni o ing o an imic obial usage including all an imic obials is no easible, a isk-based app oach should be p omo ed o a ge moni o ing o he mos
ele an an ibio ics o animal and/o human heal h and only wi hin he mos impo an animal species in a coun y o egion.
2.5. Essen ial
The choice o an imic obials o be moni o ed should be guided by he Wo ld Heal h O ganiza ion (WHO) anking o c i ically impo an an imic obials, by he Wo ld
O ganisa ion o Animal Heal h (OIE) lis o an imic obial agen s o e e ina y impo ance and by speci ic ankings o isk o public heal h om an imic obial e-
sis ance due o he use o an imic obials in e e ina y medicine (example in Table 5).
Which me ics should be employed?
2.6. Essen ial
An imic obial usage should be moni o ed a leas a he coun y le el, o all o selec ed combina ions o animal species and an imic obials.
2.7. Desi able
An imic obial usage should be moni o ed a he le el o each p esc ip ion, sale o animal adminis a ion, such as e e ina y clinics, pha macies and a ms, o all o
selec ed combina ions o animal species and an imic obials.
2.8. Essen ial
Sales da a a e he minimum ha should be p o ided o all o selec ed combina ions o animal species and an imic obials, in kilog ams o ac i e ing edien o all
animals and in millig ams pe popula ion co ec ion uni (PCU) o ood-p oducing animals.
2.9. Desi able
When da a a e a ailable on p esc ip ions, sales and animal adminis a ion, he amoun o o e all usage should be s anda dized acco ding o animal p oduc ion and
an imic obial daily doses o an imic obial ea men cou se.
Which da a and s a i ica ion c i e ia should be adop ed?
2.10. Desi able
Addi ional da a should be collec ed as pa o an an imic obial usage moni o ing such as age, p oduc ion ype, ou e o adminis a ion o ea men ype ( he apy,
me aphylaxis, p ophylaxis o g ow h p omo ion). The da a analysis should be s a i ied acco ding o hese addi ional da a.
Which c i e ia o ime in e al and epo ing should be used?
2.11. Essen ial
An imic obial usage da a should be epo ed annually.
2.12. Essen ial
Su eillance da a on an imic obial usage should be epo ed a he na ional le el.
2.13. Desi able
Su eillance da a on an imic obial usage should be epo ed a he local le el.
2.14. Essen ial
All me hods used o p o ide an imic obial usage da a should be clea ly desc ibed.
2.15. Desi able
An imic obial usage and an imic obial esis ance da a in he animal sec o should be analysed, in e p e ed and epo ed in he same epo . In he One Heal h ap-
p oach, his epo should also include da a on an imic obial usage and an imic obial esis ance om he human sec o .
2.16. Desi able
The epo should include an English e sion o os e easie sha ing o in o ma ion be ween coun ies.
Who should be he end use o he epo ?
2.17. Essen ial
The end use s o epo s on an imic obial usage should be an imic obial s ewa dship eams and all o he s akeholde s in animal, human and en i onmen al heal h
a he local, ins i u ional o indus y le el.
2.18. Desi able
The epo should be eely a ailable online o anyone and include a summa y ha is unde s andable o he gene al public.
Comp i e al.
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Table 4. An imic obial esis ance and an imic obial s ewa dship
Which animal species and esis an bac e ia should be a ge ed?
3.1. Essen ial
An imic obial esis ance should be moni o ed in ood-p oducing (including aqua ic) and companion animals.
3.2. Essen ial
The a ge esis an bac e ia should be animal pa hogens, bu also zoono ic pa hogens and commensals in he One Heal h app oach.
3.3. Essen ial
OIE c i e ia should be ollowed o he choice o animal pa hogenic bac e ia o moni o (Table 6). Examples om OIE in e es ial ood-p oducing ani-
mals a e p o ided in Table 7.
3.4. Desi able
In companion animals, a ge pa hogenic bac e ia may include me hicillin- esis an S aphylococcus au eus (MRSA) and me hicillin- esis an
S aphylococcus pseudin e medius om skin samples and Esche ichia coli om u ine samples, conside ing hei impo ance o animal heal h and
he zoono ic po en ial o MRSA.
3.5. Essen ial
Selec ion c i e ia o he oodbo ne zoono ic and commensal bac e ia o include in an an imic obial esis ance in eg a ed su eillance p og amme
should depend on public heal h p io i ies, an imic obial use p ac ices and he es ima es o he bu den o oodbo ne illnesses, as s a ed by WHO
(Table 8).
3.6. Essen ial
The choice o an imic obials o moni o should be guided by he WHO anking o c i ically impo an an imic obials, by he OIE lis o an imic obial
agen s o e e ina y impo ance and by speci ic ankings o isk o public heal h om an imic obial esis ance due o he use o an imic obials in
e e ina y medicine (example in Table 5).
How should esis ance be moni o ed?
3.7. Essen ial
Fo animal pa hogenic bac e ia, samples should o igina e om diseased o dead animals.
3.8. Essen ial
Fo indica o and zoono ic bac e ia om ood-p oducing animals, samples should be aken om heal hy animals o de ined age.
3.9. Essen ial
S anda dized and in e na ionally ecognized an imic obial suscep ibili y es ing me hods should be used.
3.10. Desi able
To suppo ield an imic obial s ewa dship eams and p o ide ecommenda ions o an imic obial he apy in e e ina y se ings, clinical b eakpoin s
should be used o in e p e an imic obial suscep ibili y es ing esul s. I no a ailable, epidemiological cu -o alues may be used. When he ob-
jec i e is o de ec dec eased suscep ibili y (i.e. o display a mic obiological esis ance), epidemiological cu -o s should be used.
3.11. Desi able
Quan i a i e da a (MICs o inhibi ion zone diame e s) should be collec ed a he han in e p e ed da a (suscep ible/in e media e/ esis ance o wild
ype/non-wild ype).
3.12. Desi able
Speci ic moni o ing schemes may be pe o med in heal hy animals and ood he eo using selec i e media, e.g. o de ec he p esence ESBL/AmpC,
ca bapenemase-p oducing, colis in- esis an En e obac e ales, MRSA o ancomycin- esis an en e ococci o assess public heal h isk.
3.13. Desi able
Resis ance mechanisms should be cha ac e ized a he molecula le el, e.g. using he polyme ase chain eac ion, sequencing o whole-genome
sequencing o colis in- esis an ESBL/AmpC- and ca bapenemase-p oducing En e obac e ales.
Which da a and s a i ica ion c i e ia should be adop ed?
3.14. Desi able
Addi ional da a should be collec ed as pa o an imic obial esis ance moni o ing, such as age, p oduc ion ype and specimen, and i he an imic o-
bial suscep ibili y es ing was eques ed due o a p e ious an imic obial ea men ailu e. The analysis should be s a i ied acco ding o hese add-
i ional da a.
Con inued
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Howe e , such da a ha e a numbe o limi a ions, such as lack o
in o ma ion on he animal species, ca ego ies (adul e sus young
animal) o be ea ed and scope o ea men s.
Rega ding he moni o ing o AMR, he online su ey highligh ed
se e al a eas o only pa ial ag eemen , such as he bac e ia o be
moni o ed. This is likely due o he complexi y o AMR moni o ing
in he animal sec o , as bo h animal and public heal h need o be
conside ed. The di e ences in design possibili ies o AMU also
apply o he moni o ing o AMR,
34,35,46,67,124
especially since i
should be done o animal bac e ial pa hogens o help in he de el-
opmen o empi ical he apy ecommenda ions in he e e ina y
se ing,
10,34,47,49
and o zoono ic and commensal bac e ia in
he One Heal h app oach.
35,36,55,68,97
This leads o e y di e en
sampling schemes: passi e moni o ing in diseased animals o
animal pa hogens and ac i e moni o ing in heal hy animals o
commensal and zoono ic bac e ia. Moni o ing sys ems may ely
on pheno ypic iden i ica ion o esis ance,bu molecula iden i ica-
ion o AMR de e minan s b ings mo e accu a e insigh s in o
he epidemiology o esis ance genes,
36,48,58,69
especially be ween
he animal and human sec o s, and can gene a e be e isk-
managemen measu es.
A speci ic challenge ha applies o he ansla ion o AMR su -
eillance da a in o AMS ac ions is he lack o clinical b eakpoin s o
in e p e an imic obial suscep ibili y es ing (AST) esul s o many
combina ions o animal species, bac e ial species and clinical
o m. The la ge majo i y o exis ing b eakpoin s we e p oduced by
he CLSI.
125
In 2019, he Ve e ina y Commi ee on An imic obial
Suscep ibili y Tes ing (Ve CAST) o he EUCAST p oposed i s i s
clinical b eakpoin s.
126
Howe e , de eloping clinical b eakpoin s is
a long and di icul p ocess, and i is unlikely ha many o he miss-
ing ones will be de e mined in he sho e m. When no b eakpoin
is a ailable, epidemiological cu -o s (ECOFFs) can be used as an
al e na i e.
36,108,114
Howe e , ECOFFs de ec dec eased suscep i-
bili ies and, as such, a e no p ope indica o s o clinical esis -
ance.
46,115
When using ECOFFs ins ead o clinical b eakpoin s,
esis ance a es can be o e es ima ed, so one should be cau ious
when p o iding ea men ecommenda ions based on hem.
46
Indeed, using ECOFFs mus no lead o w ongly ecommending
he p esc ip ion o c i ically impo an an imic obials when olde
d ugs emain clinically e icien . Because in e p e a i e c i e ia,
ei he clinical b eakpoin s o ECOFFs, can change o e ime, i is
impo an o collec and epo on quan i a i e da a (inhibi ion
diame e s o MICs) o enable he ecalcula ion o esis ance a es
in his o ical da a and s ill be able o analyse ends.
33,36,46,69,115
To ensu e ha AMR and AMU moni o ing sys ems se e AMS in
he One Heal h app oach, i is key o epo da a join ly wi h hose
o AMU and AMR in o he sec o s, especially he human one.
36,48,60
This p e en s he p o ision o a agmen ed pic u e o he AMR si u-
a ion and acili a es a ecip ocal unde s anding be ween ac o s
ha need o collabo a e o imp o e AMS. Howe e , c oss-sec o al
da a analysis o AMU and AMR da a is complex and equi es
p uden in e p e a ion. This is why expe s should always seek o
summa ize he esul s in a o ma ha is unde s andable by all
s akeholde s in animal, public and en i onmen al heal h, as well
as by he gene al public.
48
Table 4. Con inued
Which c i e ia o ime in e al and epo ing should be used?
3.15. Essen ial
The ime in e al o epo ing esis ance da a should be annual, bu eme ging esis ances should be epo ed in as imely a ashion as possible.
3.16. Essen ial
Su eillance da a on an imic obial esis ance should be epo ed a he na ional le el.
3.17. Desi able
Su eillance da a on an imic obial esis ance should be epo ed a he local le el.
3.18. Essen ial
All s anda ds and guidance documen s used o bac e ial isola ion, bac e ial iden i ica ion and an imic obial suscep ibili y es ing should be clea ly
desc ibed.
3.19. Desi able
An imic obial usage and an imic obial esis ance da a in he animal sec o should be analysed, in e p e ed and epo ed in he same epo . In he
One Heal h app oach, his epo should also include da a on an imic obial usage and an imic obial esis ance om he human sec o .
3.20. Desi able
The epo should include an English e sion o os e easie sha ing o in o ma ion be ween coun ies.
Who should be he end use s o he epo ?
3.21. Essen ial
The end use s o epo s on an imic obial esis ance should be an imic obial s ewa dship eams and all o he s akeholde s in animal, human and en-
i onmen al heal h a he local, ins i u ional o indus y le el.
3.22. Desi able
The epo should be eely a ailable online o anyone and include a summa y ha is unde s andable o he gene al public.
Comp i e al.
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Fu he opics we e explo ed and add essed as esea ch a eas
du ing consul a ions. Al hough planning dedica ed ime and allo-
ca ing speci ic measu es o AMS eams a e essen ial o AMS ac i -
i ies, de ailed in o ma ion on he minimum equi emen s o
pe sonnel acco ding o he asks o AMS p og ammes a e lacking
in he li e a u e. Addi ionally, he lack o clinical b eakpoin s o
many an imic obials o many animal species emains an impo -
an limi a ion o he in e p e a ion o AST and o guide p uden
use o an imic obials. This ep esen s he main issue ha mus be
add essed o imp o e AMS ac i i ies. Due o he lack o a ailable
documen s e ie ed o wo key ques ions and ollowing he nu-
me ous discussions among he panel, addi ional opics we e con-
side ed as impo an u u e esea ch a eas ha should be
in es iga ed and could complemen he cu en checklis . The
main esea ch p io i ies a e summa ized in Table9.
To ou knowledge, his is he i s ime ha a consensus om an
in e na ional g oup o e e ina y and medical expe s has been
eached in he e e ina y se ing ega ding AMS leade ship and ac-
coun abili y, as well as on he AMU and AMR in o ma ion ha moni-
o ing sys ems should p o ide in he animal sec o o suppo AMS
Table 5. Ca ego iza ion o an imic obials conside ing he isk o public heal h om hei usage in e e ina y medicine due o an imic obial esis ance,
by he An imic obial Ad ice Ad Hoc Expe G oup (AMEG) om he Eu opean Medicines Agency (EMA)
9
Ca ego y Lis o d ugs
Ca ego y A ‘A oid’ •Aminopenicillins
•Ca bapenems
•O he cephalospo ins (o he han 1s , 2nd, 3 d and 4 h gene a ion) and penems (ATC code J01DI),
including combina ions o 3 d-gene a ion cephalospo ins wi h b-lac amase inhibi o s
•Glycopep ides
•Glycylcyclines
•Ke olides
•Lipopep ides
•Monobac ams
•Oxazolidinones
•Penicillins (ca boxypenicillins and u eidopenicillins, including combina ions wi h b-lac amase inhibi o s)
•Phosphonic acid de i a i es
•Pseudomonic acid
•Ri amycins (excep i aximin)
•Rimino enazines
•S ep og amins
•Sul ones
•D ugs used solely o ea ube culosis o o he mycobac e ial diseases
•Subs ances newly au ho ized in human medicine ollowing publica ion o he AMEG ca ego iza ion
Ca ego y B ‘Res ic ’ •3 d- and 4 h-gene a ion cephalospo ins, excep combina ions wi h b-lac amase inhibi o s
•Polymyxins
•Quinolones ( luo oquinolones and o he quinolones)
Ca ego y C ‘Cau ion’ •Aminoglycosides (excep spec inomycin)
•Aminopenicillins in combina ion wi h b-lac amase inhibi o s
•Amphenicols
•1s - and 2nd-gene a ion cephalospo ins and cephamycins
•Mac olides (no including ke olides)
•Lincosamides
•Pleu omu ilins
•Ri amycins ( i aximin only)
Ca ego y D ‘P uden ’ •Aminopenicillins wi hou b-lac amase inhibi o s
•Cyclic polypep ides
•Ni o u an de i a i es
•Ni oimidazoles
•Penicillins (an is aphylococcal penicillins and na u al penicillins)
•Aminoglycosides (spec inomycin only)
•S e oid an ibac e ials
•Sulphonamides, dihyd o ola e educ ase inhibi o s and combina ions
•Te acyclines
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ac i i ies in he One Heal h app oach. The ini ial s ep o he li e a u e
e iew was use ul in guiding g oup discussions and inding ag ee-
men . Howe e , he subjec i e na u e o he expe s’ opinions and
he small numbe o pa icipan s emain limi a ions o he app oach.
A majo s eng h o his documen is ha i p o ides p ac ical
andconcise indica ions o AMS eams in he ield, bu also o ins i-
u ions wishing o suppo AMS om a highe le el, especially
when i ela es o he p oduc ion o AMR and AMU da a ha a e
ele an o p esc ibe s, selle s and use s o an imic obials in ani-
mals. These indica ions a e also use ul o medical doc o s wishing
o be e unde s and he speci ici ies o he e e ina y sec o in
e ms o su eillance and AMS, especially as some ac i i ies a e
designed wi h a public heal h pe spec i e. This wo k also enabled
he iden i ica ion o se e al impo an u u e esea ch a eas o a-
cili a e he de elopmen o AMS p og ammes and he ansla ion
o AMR su eillance da a in o p uden use o an imic obials in he
e e ina y se ing. Howe e , due o he di e si y and complexi y o
he e e ina y sec o , along wi h he ac ha di e se economic
con ex s we e conside ed, many a ge s o he checklis a e a he
gene ic and need o be adap ed o each speci ic con ex . In his
scena io, he indica ions gi en he ein ep esen a i s s ep o be -
e s uc u e AMS ac i i ies in he animal sec o .
Conclusions
A lis o essen ial and desi able a ge s was p oduced ollowing de-
elopmen o consensus be ween expe s om bo h medical and
Table 6. OIE c i e ia o be conside ed in he choice o animal bac e ial pa hogens o inclusion in an AMR moni o ing p og amme
a
•Impac on animal heal h and wel a e
•Implica ion o an imic obial esis ance o he animal bac e ial pa hogen on he apeu ic op ions in e e ina y p ac ice
•Impac on ood secu i y and on p oduc ion (economic impo ance o associa ed diseases)
•Bac e ial diseases esponsible o he majo i y o e e ina y an imic obial usage (s a i ied by usage o di e en classes o hei impo ance)
•Exis ence o alida ed suscep ibili y es ing me hodologies o he bac e ial pa hogen
•Exis ence o quali y assu ance p og ammes o o he pa hogen- educ ion op ions ha a e non-an imic obial, such as accines and Good
Ag icul u al P ac ices
a
Adap ed om Table 2o e e ence 33.
Table 7. OIE example o bac e ial pa hogens in e es ial ood-p oducing animals o include in an AMR moni o ing p og amme
a
Species Respi a o y pa hogens En e ic pa hogens O he pa hogens
Ca le Pas eu ella mul ocida,
Mannheimia haemoly ica
Esche ichia coli,
Salmonella spp.
Udde pa hogens
b
, such as
S aphylococcus au eus,
S ep ococcus spp.
Pigs Ac inobacillus pleu opneumoniae Esche ichia coli,
Salmonella spp.
S ep ococcus suis
Poul y – Salmonella spp. Esche ichia coli
a
Adap ed om in o ma ion in e e ence 33.
b
Re e s o pa hogens causing mas i is (mamma y gland in ec ion).
Table 8. Foodbo ne and indica o bac e ia o include in an AMR moni o ing p og amme
•In e es ial ood-p oducing animals, zoono ic bac e ia ypically include Salmonella spp. and Campylobac e spp. om caecal samples
•In e es ial ood-p oducing animals, indica o bac e ia (animal commensal bac e ia as po en ial ese oi o d ug esis ance genes) ypically in-
clude Esche ichia coli and en e ococci om caecal samples
•O he bac e ia (e.g. me hicillin- esis an S aphylococcus au eus, Clos idioides spp. and Lis e ia monocy ogenes om e es ial ood-p oducing ani-
mals o Vib io pa ahaemoly icus and Salmonella spp. om aquacul u e p oduc ion) may be included acco ding o he epidemiology o oodbo ne
diseases in he a ea
Comp i e al.
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