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A rationale to unify measurements of effectiveness for animal health surveillance

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Vladimir Grosboisa,∗, Barbara Häslerb, Marisa Peyrea, Dao Thi Hiepc, Timothée Vergneb a UPR AGIRs, Animal and Integrate Risk Management, International Research Center in Agriculture for

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Vladimir Grosboisa,∗, Barbara Häslerb, Marisa Peyrea, Dao Thi Hiepc,

Timothée Vergneb

a UPR AGIRs, Animal and Integrate Risk Management, International Research Center in Agriculture for Development (CIRAD), TA C 22/E

Campus International Baillarguet, 34398 Montpellier Cedex 5, France

b Veterinary Epidemiology, Economics and Public Health, The Royal Veterinary College, Hawkshead Lane, North Mymms, Hatfield, Herts

AL9 7TA, United Kingdom

c Center for Interdisciplinary Research on Rural Development, Vietnam National University of Agriculture, Trau Quy, Gia Lam, Hanoi,

Viet Nam

Article history:

Received 3 July 2014

Received in revised form 5 December 2014

Accepted 15 December 2014

Keywords:

Intervention

Disease surveillance

Decision making

Type I error

Type II error

Surveillancesystemsproducedatawhich,onceanalysedandinterpreted,supportdecisions regardingdiseasemanagement.Whileseveralperformancemeasuresforsurveillanceare

inuse,notheoreticalframeworkhasbeenproposedyetwitharationalefordefiningand estimatingeffectivenessmeasuresofsurveillancesystemsinagenericway.Aneffective surveillancesystemisasystemwhosedatacollection,analysisandinterpretation pro-cessesleadtodecisionsthatareappropriategiventhetruediseasestatusofthetarget population.Accordingly,wedevelopedaframeworkaccountingforsampling,testingand datainterpretationprocesses,todepictinaprobabilisticwaythedirectionandmagnitude

ofthediscrepancybetween“decisionsthatwouldbemadeifthetruestateofapopulation wasknown”andthe“decisionsthatareactuallymadeupontheanalysisandinterpretation

ofsurveillancedata”.Theproposedframeworkprovidesatheoreticalbasisfor standard-isedquantitativeevaluationoftheeffectivenessofsurveillancesystems.Weillustratesuch approachesusinghypotheticalsurveillancesystemsaimedatmonitoringtheprevalenceof

anendemicdiseaseandatdetectinganemergingdiseaseasearlyaspossibleandwithan empiricalcasestudyonapassivesurveillancesystemaimingatdetectingcasesofHighly PathogenicAvianInfluenzacasesinVietnamesepoultry

©2015ElsevierB.V.Allrightsreserved

1 Introduction

Knight-JonesandRushton,2013;Otteetal.,2004).These

∗ Corresponding author Tel.: +33 467593833; fax: +33 467593799.

E-mail address: Vladimir.grosbois@cirad.fr (V Grosbois).

Knight-JonesandRushton,2013).Importantly,tocombatanimal

http://dx.doi.org/10.1016/j.prevetmed.2014.12.014

0167-5877/© 2015 Elsevier B.V All rights reserved.

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management

et al., 2011; Drewe et al., 2012,2015; Hoinville et al.,

2007a).Such evaluationforsystemsaimingatdetecting

Yamamotoetal.,2008;Knight-Jonesetal.,2010).Finally,

2 General overview of the rationale

variables

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SURVEILLANCE DATA Non-exhausve, non-representave, parally distorted

ASSESSMENT EPIDE MIO LOGICA L SITUATION

PREVEN TIO N/CONTROL MEASURES

That are actually implemented (modalies/intensity)

TRUE EPIDE MIO LOGICA L SITUATION

PREVEN TION/ CONTROL MEASUR ES

That would be implemented given a

perfect knowledge of the epidemiological situaon

Data ana lysis an d interpr etaon

Decision making proc ess

Intervenon strategy

Definedbasedon epidemiological modellingand cost-effecveness and/or cost-benefitanalyses

Data genera on proc ess

Sampling, reporng, diagnosing, tesng

EFFECTIVEN ESS AN D ECONOMIC EFFICIENCY of the risk prevenon/control measuresthatare actually implemented

EFF ECT IVEN ESS AND ECONOMIC

EFFICIENCY

of the prevenon/controlmeasures

that would be implemented given a perfect knowledge of the

epidemiological situaon

Surveilla nce Effecve nes s

Fig 1. Proposed approach for the evaluation of the effectiveness of a surveillance system.

Table 1

Examples of simple intervention strategies for various surveillance objectives.

Surveillance

objective

Monitoring

prevalence

Country/region Yearly

prevalence of a disease (Prev)

Prev ≤ Threshold Do nothing Prev > Threshold Implement

systematic testing in slaughter-houses before products are put on the market Disease case

detection

Herd Disease status No infected

animal in the herd

Do nothing ≥1 infected

animal in the herd

Cull the herd

Demonstrate

freedom

from disease

Country/region Yearly

prevalence of a disease (Prev)

Prev ≤ Threshold Allow

exportations

Prev > Threshold Ban

exportations Early detection

of an

emerging

disease

Country/region Instantaneous

incidence rate (IIR)

IIR = 0 Do nothing IIR > 0 Launch

intensive surveillance and in depth case investigation Limit movements

S−, S + : epidemiological states for which the “no intervention” and “intervention” options, respectively, are required; I−, I + : description of actions associated with to the “no intervention” and “intervention” options.

formthebasisforaninterventiondecision.Therelevant

epidemiologicalscaleisthescaleatwhichdecisionsare

being made about implementing an intervention Such

decisionscanbeforexampletostartvaccinatinganimals

inthetargetpopulationifthediseaseprevalencecrosses

adefinedthresholdornottodoanythingifsurveillance

todocumentfreedomfromdiseasedeliverstheexpected result(i.e.freedom).Thescalecanbeanimal,herd,country,

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regional orglobal level.The relevant statevariable isa

variable, such as prevalence or incidence, that reflects

the current epidemiological situation, and which value

determines the intervention measures considered as

appropriatebystakeholdersanddecisionmakers.Table1

(Tomassenetal.,2002)

processes

response

3 Illustrations of effectiveness assessment three contrived surveillance system examples and an empirical case study

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Table 2

Examples of decision making rules relying on the analysis and interpretation of surveillance data The decision rules correspond to the mitigation strategies presented in Table 1

Surveillance

objective

Scale Statistics used

to assess epi-demiological status

Monitoring

prevalence

Country/region Proportion of

positive tests in the samples collected over a year P(+)

P(+) ≤ Threshold Do nothing P(+) > Threshold Implement

systematic testing in slaughter-houses before products are put on the market Case detection

of disease

Herd Result of a

pooled test

Negative test result

Do nothing Positive test

result

Cull the herd Demonstrate

freedom

from disease

Country/region Proportion of

positive tests in the samples collected over a year P(+)

P(+) ≤ Threshold Allow

exportations

P(+) > Threshold Ban

exportations

Early detection

of an

emerging

disease

Country/region Case reporting No case

reported

Do nothing ≥1 case

reported

Launch intensive surveillance and in depth case investigation Limit movements

A − , A + : assessments of epidemiological state for which the “no intervention” and “intervention” options, respectively, are implemented; I − , I + : description

of actions associated with the “no intervention” and “intervention” options.

Table 3

The two types of error used as effectiveness criteria.

True epidemiological status

S + intervention required S−intervention not required Assessment of the epidemiological status resulting from the generation, analysis and interpretation of surveillance data

A − intervention not implemented Type II error

S − , S + : epidemiological states for which the “no intervention” and “intervention” options, respectively, are required; A − , A + : assessments of epidemiological state for which the “no intervention” and “intervention” options, respectively, are implemented.

variablewhichconditions decisionsinterms of

preven-tion/interventionmeasures is usually the prevalenceof

thediseaseinthefocalpopulation.Theprevalence

cate-goriesconsideredasrequiringdistinctinterventionoptions

aredeterminedaccordingtothesocalled“design

preva-lence”.Whenevertheprevalenceinthepopulationisbelow

thedesignprevalence,theterritoryisconsidered“asfree

fromthedisease”(S−)andnomeasuretolimititsspread

is implemented (for instance no limitations to animal

trading:I−)whereaswhenevertheprevalenceinthe

pop-ulationisabovethedesignprevalence,measurestolimit

itsspreadareimplemented(forinstanceanimaltradingis

restricted:I+).Thecrucialaspectofthemitigation

strat-egyisthedeterminationofthedesignprevalence.Itcan

bechosenbasedontherelativelikelihoodofprevalence

levelsgiven thepresenceofthediseaseontheterritory

orbyconsideringhowthemagnitudeofsanitaryand

eco-nomicconsequences ofthepresenceofthediseasevary

as a function of the prevalenceof that disease So the

designprevalencecanbetheminimumexpected

preva-lenceofthediseaseprovideditispresentontheterritory

orthemaximumprevalenceatwhichthesanitaryand eco-nomic consequences of thepresence of thedisease are consideredasnegligible.Thestatisticsusedtoassessthe epidemiological situationfrom surveillancedata is usu-allythebinaryvariablereflectingwhetheratleastonecase hasbeendetected(A+)ornocasehasbeendetected(A−)

Inthenumerouspapersinwhichthisapproachhasbeen used toassess theeffectiveness ofsurveillance systems aimingatdemonstratingthefreedomofaterritoryfrom

adisease(e.g.Martinetal.,2007a;Martin,2008;Frössling

etal.,2009;Hoodetal.,2009;Christensenetal.,2011),the

(Martinetal.,2007b)althoughothermethodshavebeen

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Table 4

Information for assessing the effectiveness of a contrived surveillance system aiming at monitoring the prevalence of an endemic disease.

Surveillance

objective

Knowing how prevalent is an endemic disease to inform decisions about vaccination strategy

Relevant scale Country (population of 100,000

animals) Relevant

epi-demiological

variable

Individual level prevalence (p)

Intervention strategy S−

p ≤ 0.1

S +

0.1 < p ≤ 0.2

S ++

p > 0.2

I −

no vaccination

I +

vaccination is implemented only in high risk areas

I ++

vaccination is implemented

in all areas

Surveillance

data

generation

process

n = 100 randomly chosen individuals are sampled over a

1 month period (coverage = 0.1%) Each sample

is tested using a test with sensitivity Se = 0.90 and specificity Sp = 0.95 Statistics

computed

from

surveillance

data

Number of sampled units testing positive (n p )

Decision rule 1 (test performances

not accounted for)

A −

n p ≤ 0.1 * n

A +

0.1 * n < n p ≤ 0.2 * n

A ++

n p > 0.2 * n

I −

no vaccination

I +

targeted vaccination is implemented

I ++

vaccination is implemented

in all areas Decision rule 2 (test

performances accounted for)

A−

n p ≤ (0.1 * Se + (1 − 0.1) * (1 − Sp)) * n

A +

(0.1 * Se + (1 − 0.1) * (1 − Sp)) * n

<n p ≤ (0.2 * Se + (1 − 0.2) * (1 − Sp)) * n

A ++

n p > (0.2*Se + (1 − 0.2)*(1 − Sp)) * n

I −

no vaccination

I +

targeted vaccination is implemented

I ++

vaccination is implemented

in all areas

S − , S + , S ++ : epidemiological states for which the “no intervention”, “low intensity intervention” and “high intensity intervention” options, respectively, are required; I−, I + , I ++ : description of actions associated with the “no intervention”, “low intensity intervention” and “high intensity intervention” options, respectively; A−, A + , A ++ : assessments of epidemiological state for which the “no intervention”, “low intensity intervention” and “high intensity intervention” options, respectively, are implemented.

3.2 Monitoringtheprevalenceofanendemicdisease

This section presents a contrived example an active

surveillancesystemaimingatmonitoringprevalenceofa

cattlediseasetoinformdecision-makersonwhich

vacci-nationstrategytoimplementatthenationallevel

3.2.1 Informationrequiredforassessingeffectiveness

Table4summarisestheinformationrequiredtoassess

(Table4).Thedatainterpretationprocessconsistsin

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Fig 2.Probabilities that data generation, analysis and interpretation processes result in the implementation of different intervention options as a function

of the true epidemiological state n: sample size; Se: sensitivity of the test; Sp: specificity of the test; S−: vaccination is not required; S + : targeted vaccination

is required; S ++ : mass vaccination is required.

0.68

rule1inTable4).InFig.4 testsensitivityandspecificity

system

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Fig 3.Sensitivity of surveillance effectiveness to changes in sampling and sample testing procedures n: sample size; Se: sensitivity of the test; Sp: specificity

of the test.

Fig 4. Sensitivity of surveillance effectiveness to changes in data analysis and interpretation procedures n: sample size; Se: sensitivity of the test; Sp: specificity of the test.

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Table 5

Information for assessing the effectiveness of a contrived surveillance system aiming at detecting an emerging or exotic disease early.

Surveillance objective Detecting an emerging disease

following its introduction in a territory as soon as possible Relevant scale Country (population of 10,000

animals) Relevant epidemiological variables Cumulative incidence

(correlated with time elapsed since introduction and spatial spread)

Intervention strategy S−Thediseasehasnotyetbeen

introduced

S + The disease has been introduced but cumulative incidence is <0.5%

S ++ Cumulative incidence is

≥0.5%

I − Keep low intensity surveillance with 50 individuals sampled daily

I + Cull detected infectious cases and reinforce surveillance with

100 individuals sampled daily

I ++ Cull detected infectious cases, reinforce surveillance with 200 individuals sampled daily, and limit animal movements Surveillance data generation process Randomly chosen individuals

are sampled daily Samples are screened for antibody using a test which sensitivity is Se = 0.8 and specificity is Sp = 1.

Seropositive samples are tested for pathogen detection using a test which sensitivity and specificity are 1 Statistics computed from surveillance data Cumulative number of

detected cases (n p )

− No case detected so far A + One case detected A ++ At least two cases detected

I − Keep low intensity surveillance with 50 individuals sampled daily

I + Cull the case if it is infectious and reinforce surveillance with

100 individuals sampled daily

I ++ Cull detected infectious cases, reinforce surveillance with 200 individuals sampled daily, and limit animal movements

S − , S + , S ++ : epidemiological states for which the “no intervention”, “low intensity intervention” and “high intensity intervention” options, respectively, are required; I − , I + , I ++ : description of actions associated with the “no intervention”, “low intensity intervention” and “high intensity intervention” options, respectively; A−, A + , A ++ : assessments of epidemiological state for which the “no intervention”, “low intensity intervention” and “high intensity intervention” options, respectively, are implemented.

importantepidemiologicalstatevariablessuchas

cumu-lativeincidence, spatial spread, and averagenumber of

transmission eventsthat link a case to the index case

Astime elapsedsince theoccurrence of theindex case

increasessodocumulativeincidenceandspatialspread

Consequently,thelatertheimplementationofintervention

measures(relativetothetimeofoccurrenceoftheindex

case)thelargerarethelossesalreadygeneratedbythe

dis-ease.Thisalsomeansthatcostsofinterventionmeasures

requiredwillincreasewithmoreanimalsand/orholdings

beingaffected

Theperformance of a surveillance system aimingat

detectinganemergingpathogenasearlyaspossiblecould

thusbeevaluatedaccordingtotwocomponents:its

abil-itytodetectatanypointintimethepresenceofthefocal

pathogeninthefocalhostpopulationanditsabilityto

eval-uatethespatialspreadandprevalenceofthefocalpathogen

onceitspresencehasbeendetected.Thefirstcomponent

is probably the most important because a surveillance

systemwhich performs well in terms of instantaneous

detectionprobabilitywillallowimplementationof

preven-tion/controlmeasuressoon aftertheintroductionofthe

pathogen,whenthelossesalreadygeneratedbythedisease

aswellastheresourcesrequiredformitigationmeasuresto

controlitsfurtherspreadarelimited.Thesecondcriterion

reflectstheabilityofthesurveillancesystem,once detec-tionhasbeenachieved,toprovideinformationthatallows theimplementationofmitigationmeasureswhichnature and intensitywouldbeconsideredasadaptedby stake-holdersanddecisionmakersgivenperfectknowledgeof therealepidemiologicalsituationintermsofprevalence andspatialspread.Thissecondcomponentisrelatestothe evaluation ofsurveillancesystemsaimingatmonitoring theprevalenceofadisease.Suchattributesarepresented

inSection3.2

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Fig 5. Effectiveness of a contrived surveillance system aiming at detecting the introduction of an emerging disease as early as possible.

processes

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