Exploration of risk factors contributing to the presence of influenza A virus in swine at agricultural fairs.

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by  Bowman, Andrew S

EmergingMicrobesandInfections(2014)3,e5;doi:10.1038/emi.2014.5
OPEN (cid:2)2014SSCC.Allrightsreserved2222-1751/14
www.nature.com/emi
ORIGINAL ARTICLE
Exploration of risk factors contributing to the presence of
influenza A virus in swine at agricultural fairs
AndrewSBowman1,JeffreyDWorkman1,2,JacquelineMNolting1,SarahWNelson1andRichardDSlemons1
InfluenzaAvirusinfectionsoccurringinexhibitionswinepopulationsatagriculturalfairsduring2012servedasasourceofH3N2variant
influenzaAvirusestransmittedtohumansresultinginmorethan300documentedcases.Priortotheoutbreak,thisinvestigationwas
initiatedtoidentifyfair-levelriskfactorscontributingtoinfluenzaAvirusinfectionsinpigsatagriculturalfairs.Aspartofanongoing
activesurveillanceprogram,nasalswabsandassociatedfair-levelmetadatawerecollectedfrompigsat40juniorfairmarketswineshows
heldinOhioduringthe2012fairseason.AnalysesofthedatashowthattheadjustedoddsofhavinginfluenzaAvirus-infectedpigsata
fairwere1.27(95%confidentialinterval(CI):1.04–1.66)higherforevery20pigincreaseinthesizeoftheswineshow.Additionally,four
ofthefivefairsthathostedbreedingswineshowsinadditiontotheirjuniorfairmarketswineshowshadpigstestpositiveforinfluenzaA
virus.Whilethecurrentstudywaslimitedto40fairswithinonestate,thefindingsprovidedinsightforveterinaryandpublichealth
officialsdevelopingmitigationstrategiestodecreasetheintra-andinter-speciestransmissionofinfluenzaAvirusatfairs.
EmergingMicrobesandInfections(2014)3,e5;doi:10.1038/emi.2014.5;publishedonline22January2014
Keywords: H3N2v;influenza;swine;zoonoticdisease
INTRODUCTION Reported cases of humans contracting IAV infections directly or
The comingling of swine from numerous premises with varied indirectly from pigs have beenhistorically sporadicand these variant
managementpracticesandtheirinteractionwithlargenumbersofexhi- IAVsshowedlimitedcapabilityforsustainedhuman-to-humantrans-
bitorsandvisitorsmakeagriculturalfairsanidealsettingfortheintra- mission.12–14However,theemergenceoftheinfluenzaA(H1N1)pdm09
and inter-species transmission of influenza A viruses (IAVs) between virus, a strain containing gene segments from North American and
swine and human populations.1,2 The frequency with which intra- Europeanswinelineages,15illustratedthepandemicpotentialofswine
and inter-species IAV transmission occurs in these settings is likely lineage IAVs crossing the species barrier to humans. While
duetoamyriadoffactors,includingbutnotlimitedto,management A(H1N1)pdm09 rapidly spread worldwide and became endemic in
practices,IAVstrain,andanimaland/orhumanpopulationimmunity. thehumanpopulation,16sequencingofthisvirushastodatefailedto
SwineisahostspeciesinwhichreassortmentofIAVgenomicsegments elucidate any virulence or adaptation markers that would explain its
mayleadtoemergentnovelstrains,sincetheyaresusceptibletoinfection human-to-humantransmissionefficiency,highlightingourinabilityto
from swine, human and avian influenza A viruses.3,4 For this reason, predict IAVs with pandemic potential. While the origin of the
limitingthebidirectionalzoonotictransmissionofthesevirusesatagri- A(H1N1)pdm09virusremainsunknown,theviruswasintroducedinto
culturalfairsisimportantforpublicandanimalhealth. theNorthAmericanswinepopulationin2009andhassincereassorted
The association between human and swine influenza was reported withotherswine-originIAVs.17,18
afterrespiratorydiseasesimilartothehumandiseasewasnotedinpigs EpidemiologicaldatashowthatzoonotictransmissionofIAVfrom
duringthe1918humanSpanishflupandemic.5H1N1IAVsubsequently swine to humans has been documented at unprecedented levels in
becameestablishedintheUnitedStatesswinepopulationwiththerelat- recent years. More than 320 human cases of infection with variant
ednessoftheswineandhumanvirusesbeingestablishedin1931.6For IAVs were reported to the Centers for Disease Control 2011–201219
nearly80years,classicalswineinfluenzaH1N1viruswasthedominant andlikelythousandsmoreH3N2vcaseswentunreportedduringthose
endemicIAVstrainintheNorthAmericaswinepopulation.7In1998, years.20ThesezoonoticIAVscontainedsevengenesfromcontemporary
triple reassortant H3N2 IAVs containing polymerase basic 1 (PB1), NorthAmericanswinelineageIAVandonegene(M)derivedfromthe
hemagglutinin (HA) and neuraminidase (NA) gene segments from H1N1pdm09 virus.21,22 The majority of the cases were epidemiologi-
humanIAVlineages,polymerasebasic2(PB2)andpolymeraseacidic cally linked to swine exposure occurring at agricultural fairs across
(PA) genes from avian lineages, and nucleoprotein (NP), matrix (M) severalstates.19,23–25WithinOhio,107H3N2vcasesdocumenteddur-
andnon-structural(NS)genesegmentsfromswinelineages,emergedin ing2012resultedinelevenhospitalizationsandonefatality.26Wereco-
NorthAmericanswine.8Subsequently,thislineagebecameestablishedin veredIAVfromexhibitionswineat10of40(25%)Ohiofairssampled
USandCanadianswineherdsandhasresultedinanincreasedrateof during2012.GenomicanalysesofH3N2IAVisolatesrecoveredfrom
geneticandantigenicchangeamongswine-originIAVs.9–11 pigs at one agricultural fair in the state during 2012 demonstrated
1DepartmentofVeterinaryPreventiveMedicine,CollegeofVeterinaryMedicine,TheOhioStateUniversity,Columbus,OH43210,USAand2OhioStateUniversityExtension,The
OhioStateUniversity,Columbus,OH43210,USA
Correspondence:ASBowman
E-mail:[email protected]
Received5October2013;revised3December2013;accepted5December2013
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.99%nucleotidesimilaritytoH3N2visolatesrecoveredfromconcur- proportions and the Kruskal–Wallis equality-of-populations rank
renthumancases,providingmolecularconfirmationofzoonoticIAV testwasusedforcontinuousvariables.Univariateanalysiswasper-
transmission.2ThisrecordnumberofvariantinfluenzaAcasescreated formed to calculate unadjusted odd ratios to identify factors con-
theneedfora‘onehealth’efforttominimizeintra-andbidirectional tributing to the presence of IAV in pigs at fairs. Exact logistic
inter-species IAV transmission at swine exhibitions.27 The reason to regression was used for multivariable modeling using a forward
prevent IAV infections among swine at fairs is clear; however, the stepwise model building approach. A cutoff of Pf0.05 was used
paucity of scientific evidencemakes it difficult for veterinary officials for inclusion in the model.
tomakesoundrecommendationstoprotectpublicandanimalhealth.
Inthepresentstudy,weinvestigatefairspecificriskfactorscontributing RESULTS
totheemergenceofinfluenzaAvirusinexhibitionswinethatcouldbe
InfluenzaAviruswasrecoveredfrompigsat10ofthe40fairsincluded
alteredtomitigatetheriskofIAVtransmissioninthesesettings. intheinvestigation.ThepresenceorabsenceofIAVinfectionamong
thepigsatthefairscouldnotbeassociatedwithcountypopulation,
MATERIALSANDMETHODS county swine inventory and number of people attending the fair
AspartofanongoingactiveIAVsurveillanceproject,swinenasalswabs (Table1).AllIAV-positivefairsand27of30(90%)negativefairswere
andassociatedmetadataaboutmanagementpracticeswerecollectedat mixedsex(barrowsandgilts)marketswineexhibitions.Theaverage
40 Ohio fairs in 2012. Molecular and microbiological assays for IAV spaceperpigatthestudiedfairswas12.8ft2/pig.Properlyfunctioning
wereperformedontheswabsaspreviouslyreported.28Samplesizewas hand-washand/orhand-sanitizerstationswereavailableat25of40
selected to provide a 95% probability of detecting IAV infection if (62.5%)fairs.Averagedailymeantemperaturewasalmost46Chigher
greaterthan15%ofthepigsateachfairwereinfected.29Allpigssampled forfairswithIAV-positivepigs(Table1).Pre-fairtag-inand/orweigh-
in this study were from junior fair market swine shows occurring at in events were rather common with 23 out of 40 (57.5%) of the
agricultural fairs. For the outcome of interest, a fair was considered enrolledfairsholdingoneoftheseevents.Foreveryincreaseof20pigs
positiveifviableIAVwasrecoveredfromoneormorepigsatthefair. atafair,theoddsratioofIAVinfectioninthepigsincreasedby1.27
Datacollectionfocusedonfairlevelvariablespossiblycontributing times(Table2).
tothepresenceorabsenceofIAVinthepigsateachexhibition.Junior
fairshowsarelimitedtolocalexhibitorsapproximatelynineyearsof DISCUSSION
agethrough19yearsofageparticipatingin4-H,FFAoranotheryouth Theresultsofthecurrentstudyprovidethefirstlookatfair-levelrisk
organization,whereasopen-classshowsaregenerallyopentoallpar- factors associated with IAV infections in swine at agricultural fairs.
ticipants regardless of age, affiliation or residence. Classification of WhileitislikelyimpossibletocompletelypreventIAVtransmissionat
swineincludedmarketswine(pigsbred,raisedandintendedforfood swine exhibitions, these data can be used to develop and evaluate
purposes)andbreedingswine(gilts,sowsand/orboarsbeingraised mitigationstrategiestoreducetheimpactofintra-andinter-species
forbreedingpurposes).Terminalswineshowsarethoseinwhichall IAV infections at swine exhibitions. Just like all other agriculture
participatinglivestockareconsignedtoharvestimmediatelyfollowing biosecurityprograms,mitigationstrategieswhicharepractical,user-
theexhibitionandpartialterminalshowsusuallyrequirethecham- friendly,lowcostanddonotdramaticallyalterthefairexperiencefor
pionanimalstobeharvestedfollowingtheexhibitionandotherpigs exhibitorsandvisitorsaremostlikelytobeconsidered,implemented
mayormaynotgotoharvest. andmaintained.
Toaccountforthevariabilityofarrivalanddepartureprocedures Notsurprisingly,largerpigshowsappeartobemorelikelytohave
amongfairsenrolledinthisstudy,thelengthoftheswineexhibition IAV-infected pigs than smaller swine exhibitions (Table 2). Larger
wasdefinedasthenumberofdaysbetweentherequiredarrivaldead- swine exhibitions tend to also have open-class and breeding swine
lineforthepigsandthedaythepigsweresampled.Studyteammem- shows in addition to junior market shows. While open-class shows
berscalculatedtheareaperpig(ft2/pig)fromtherecordedsizeofthe werecommonamongourstudiedfairs(16ofthe40),only5ofthe40
pensandthenumberofpigsperpen.Whileonthefairgrounds,study (12.5%)fairsinthisstudyhadabreedingshow;4ofthose5(80%)fairs
teammembersalsodocumentediftherewasaneasilyidentifiableand had IAV-infected pigs at the fair. The small number of fairs with
operational hand-wash and/or hand-sanitizer station within close breedingshowsinthisstudymakesanalysisofthisriskfactorprob-
proximitytotheswinebarn(s).Thesesanitationstationswereused lematic;however,thefindingisenoughtowarrantconcerngiventhat
bystudyteammemberstodetermineiftheywerefunctional. breedingswineareintendedtoleavetheexhibitionandenteraherd
Additionalvariablesincludedthenumberofpigsatthefair,number forprogenyproduction.Thisfair-to-farmmovementofpigsisadis-
ofswineexhibitors,fairattendance(numberofpeople)andvaccine easeintroductionriskforthereceivingherdandapotentialmethodto
requirements,allofwhichwerereportedtothestudyteambythefair disseminateIAVstrainsacrossalargergeographicarea.
organizers. Fair officials also reported if there was a commingling Previous research has shown that environmental stressors (heat,
event, such as a pre-fair animal identification or weighing session, lackofspace,noise)onpigscanaffectthecourseofvariousdiseases
duringtheweeksormonthspriortothefair.Exhibitiondirectorsalso incommercial swineoperations.31 The averagespace per pigatthe
reportediftherewereotherpigsbesidestheexhibitionswineonthe studiedfairswaswellabove6–8ft2/finishingpigcommonthroughout
fairgrounds(i.e.,pettingzoo,pigraces,educationaldisplays). theswineindustry.32Theresultsindicatethatheatstresscouldbea
ThecommercialswineinventorywasretrievedfromUnitedStates contributing factor to IAV infections in exhibition swine; however,
DepartmentofAgriculture’s2007CensusofAgriculture.30Thecounty cautionmustbeusedwheninterpretingthisresultbecausethevast
humanpopulationwasdefinedasthevaluereportedinthe2010US majority of the fairs with IAV-positive pigs occurred in a 4-week
censusreport.WeatherdatawerecollectedfromtheNationalWeather period during the middle of summer. This trend of mid-summer
Service’sweatherstationnearesttoeachfairground. IAVactivityinOhio’sexhibitionswinewasalsoobservedinthepre-
DatawereanalyzedusingSTATAVersion11.1(StataCorp,College viousthreeyears1andcouldbemorerelatedtoanimaland/orpeople
Station,TX,USA).Fisherexacttestwasusedtoassessdifferencesin movement between these fairs than the weather. Environmental
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Table1 SummarystatisticsandcrudeoddsratiosforpresenceofinfluenzaAvirusinpigsatfairs
Flu(1)(cid:2)xx Flu(–)(cid:2)xx Pvalue Oddsratio 95%CI
Commercialswinepopulation(31000) 11.83 43.89 0.08 0.96 0.92–1.01
Countypopulation 202255.7 70490 0.71 1.00 0.99–1.01
Numberofexhibitors 253.1 146.446 0.01 1.01 1–1.02
Numberofpigs 407 217.5667 0.01 1.01 1–1.02
Lengthofexhibition 5.2 5.33 0.64 0.89 0.45–1.75
Countyfairattendance 129180.2 80175.79 0.52 1.00 0.99–1.01
Pigspace(ft2/pig) 13.5 12.56 0.15 1.13 0.87–1.48
Averagedailymeantemperature(6C) 24.22 20.67 0.03 1.32 1.01–1.75
n % n % Pvalue Oddsratio 95%CI
Isthereabreedingshowinadditiontothejuniormarketshow?
Yes 4 40 1 3.3 ,0.001 43.5 4.1–461.79
No 6 60 29 97.7
Isthereanoperationalhand-sanitizerorhand-washstationneartheswinebarn?
Yes 6 60 19 63.3 1 0.86 0.2–3.77
No 4 40 11 36.7
Isthejuniormarketswineshowterminal?
Yes 4 40 22 73.3 0.12 0.24 0.05–1.09
No 6 60 8 26.7
Open-classswineshowinadditiontothejuniormarketshow?
Yes 7 70 9 30.0 0.06 4.67 0.99–22.01
No 3 30 21 70.0
Sexrequirementsofjuniormarketswine
Barrowsonly 0 0 3 10.0 0.56 N/A
Barrowsandgilts 10 100 27 90.0
Showmanshipoccursseparatefromthejuniormarketshow?
Yes 10 100 21 70.0 0.08 N/A
No 0 0 9 30.0
Pre-fairtag-in/weigh-in
Yes 4 40 19 63.3 0.27 0.39 0.09–1.67
No 6 60 11 36.7
Areanyswinevaccinesrequired?
Yes 0 0 1 3.3 1 N/A
No 10 100 29 97.7
Arethereotherpigsonthefairgrounds?
Yes 6 60 12 40 0.30 2.25 0.52–9.7
No 4 40 18 60
temperaturefailedtomeettheselectioncriteriaforinclusioninthe Activerecruitmentoffairswithmorediversemanagementpracticesis
finalmultivariablemodel. neededtostudytheimpactofashortenedswineexhibition.Nomatter
Whilethemajorityoffairshadhandhygienestations,theirpresence thelengthoftheexhibitiontime,thedispositionofthepigsfollowing
at fairs was not linked to the occurrence of IAV among pigs at the theshowmustbeconsidered.Themajorityoffairsinthisstudy(65%)
respectivefairs.ThelargenumberofH3N2vinfectionslinkedtoswine hadterminaljuniormarketshows.Thepracticeofhavingaterminal
exposureatagriculturalfairsduring2012suggeststhathandhygiene showwasnotassociatedwithdecreasedoddsofIAV;however,sending
stationsalsohadminimalimpactonzoonotictransmissionofIAVin allthepigstoharvestattheendofeachfairisexpectedtohelpprotect
thesesettings.However,handhygienestationsarecriticallyimportant subsequentfairsbydecreasingthepotentialforfair-to-fairspreadof
inprotectinghumanhealthbycontrollingzoonoticdiseasestransmit- IAV.
tedviadirectcontactatthesevenues.33 Mandatedvaccinationswerealmostnon-existentwithonlyonefair
One potential mitigation strategy that has been proposed is to inthecurrentstudyrequiringthepigsbevaccinatedforErysipelothrix
shorten the exhibition period.34 This would limit the time for IAV rhusiopathiaepriortothefair;nofairsrequiredthepigstoreceiveIAV
tospreadamongsusceptiblepigsanddecreasethetimehumansare vaccinationbeforearrival.UseofIAVvaccineinexhibitionswineto
exposed to IAV-infected pigs. The length of the exhibitions in the decreasetheriskofIAVinfectionsinswineandhumanshasbeenone
current study was similar between IAV-positive and -negative fairs. of the most debated topics following the H3N2v outbreak of 2012.
There are currently several commercially available swine influenza
vaccines in the United States, all of which are universally indicated
Table2 Adjustedoddsratiosfrommultivariableexactlogisticregres-
sionmodel toreduceclinicalsignsofdiseaseinpigsbutappeartohavelimited
efficacyagainst2012H3N2vstrains.35Althoughtheirimpactonintra-
Adjustedoddsratio Pvalue 95%CI
and inter-species transmission dynamics remains unclear,36 it is
Breedingshow 21.676 0.005 2.417–‘ expected that IAV vaccines will impart at least partial immunity to
Numberofpigs 1.012 0.012 1.002–1.026 circulating strains of IAV, which should decrease viral shedding
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duringafair.AnunintendedconsequenceofIAVvaccineusemaybe ACKNOWLEDGMENTS
vaccine-associated enhanced respiratory disease, which has been Wethankourcollaboratorsfromtheparticipatingagriculturalfairs.Wealso
reportedinswinevaccinatedwithswineinfluenzavirusvaccinesthat thankWendellBliss,GaryBowmanandDimitriaMathys(TheOhioState
aremismatchedtocirculatingstrains.37Furthermore,decreaseofclin- University,USA)andTonyForshey(OhioDepartmentofAgriculture,USA)
fortheirassistanceandsupportwiththisproject.Thisworkhasbeenfundedby
icalsignsmayhamperrecognitionandresponsetoactiveIAVinfec-
theMinnesotaCenterofExcellenceforInfluenzaResearchandSurveillance
tionsinexhibitionpigs.
withfederalfundsfromtheCentersofExcellenceforInfluenzaResearchand
SomeofthemajorpitfallsofmandatedIAVvaccinationliewiththe
Surveillance,NationalInstituteofAllergyandInfectiousDiseases,National
practicalapplicationofvaccinesinthissetting.Thelogisticsofvaccine InstitutesofHealth,DepartmentofHealthandHumanServices,under
distributiontoswineexhibitorspriortothefairbecomesdifficultbecause contractNOHHSN266200700007C.
mostexhibitionswineareraisedbyyouthexhibitorsinsmall,dispersed
herds(,10pigsperherd).Commercialvaccinesareusuallysoldino50
dosesperbottleaddingtothecostpervaccinatedpiginthesesmallherds.
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