HAL Id: hal-01452897
https://hal.univ-reunion.fr/hal-01452897
Submitted on 27 Jun 2018
HAL is a multi-disciplinary open access
archive for the deposit and dissemination of
sci-entific research documents, whether they are
pub-lished or not. The documents may come from
teaching and research institutions in France or
abroad, or from public or private research centers.
L’archive ouverte pluridisciplinaire HAL, est
destinée au dépôt et à la diffusion de documents
scientifiques de niveau recherche, publiés ou non,
émanant des établissements d’enseignement et de
recherche français ou étrangers, des laboratoires
publics ou privés.
Distributed under a Creative Commons Attribution - NonCommercial - NoDerivatives| 4.0
International License
Silent Circulation of Ross River Virus in French
Polynesia
Maïté Aubry, Jérôme Finke, Anita Teissier, Claudine Roche, Julien Broult,
Sylvie Paulous, Philippe Desprès, Van-Mai Cao-Lormeau, Didier Musso
To cite this version:
Maïté Aubry, Jérôme Finke, Anita Teissier, Claudine Roche, Julien Broult, et al.. Silent Circulation
of Ross River Virus in French Polynesia. International Journal of Infectious Diseases, Elsevier, 2015,
37, pp.19-24. �10.1016/j.ijid.2015.06.005�. �hal-01452897�
Silent
Circulation
of
Ross
River
Virus
in
French
Polynesia
Maite
Aubry
a,*
,
Je´roˆme
Finke
b,
Anita
Teissier
a,
Claudine
Roche
a,
Julien
Broult
c,
Sylvie
Paulous
d,
Philippe
Despre`s
d,e,
Van-Mai
Cao-Lormeau
a,
Didier
Musso
aa
UnitofEmergingInfectiousDiseases,InstitutLouisMalarde´,POBOX30,98713Papeete,Tahiti,FrenchPolynesia
b
HochschuleEmden/Leer,Constantiaplatz4,D-26723Emden,Germany
c
CentredeTransfusionSanguinedelaPolyne´siefranc¸aise,HoˆpitalduTaaone,POBOX4530,98713Papeete,Tahiti,FrenchPolynesia
dDepartementInfectionsandEpidemiology,InstitutPasteur,75724Paris,France
eUMRPIMIT(12T)Universite´ deLaRe´union,INSERMU1187,CNRS9192,IRD249,GIP-CYROI,97491Sainte-Clotilde,France
1. Introduction
FrenchPolynesia(FP)isa Frenchoverseas territoryof about 270,000 inhabitants in the Southeast Pacific, and one of the 22 Pacific Islands Countries and Territories (PICTs). Arthropod-bornevirus(arbovirus)infectionsaremajorpublichealthconcern in the PICTs, with dengue virus (DENV), a Flavivirus of the Flaviviridae family, as the mostcommon circulating and wide-spreadarbovirus.1InFP,DENVoutbreakshavebeenrecordedsince
the 40s.1–4 DENV used to be the only arbovirus isolated until
October2013whenFPexperiencedthelargestoutbreakofZika virus (ZIKV) ever reported,5,6 followed by an outbreak of
chikungunyavirus(CHIKV)thatstartedinOctober2014.7These
two viruses, belonging respectively toFlavivirus and Alphavirus
genera,have also beenrecently involved in outbreaksin other PICTs.6,8,9OtherarboviruseshavebeenreportedinPICTs,butnotin
FP,suchasJapaneseencephalitisvirus(JEV)10andRossRivervirus
(RRV).11
RRVisanarbovirusbelongingtotheAlphavirus genusofthe Togaviridae family.12 It was first isolated from Aedes vigilax
mosquitoes in Australia in 195913 and further frommore than
30mosquitospecies.12Themostcommonclinicalmanifestations of RRV infections are fever, arthralgia and rash.Asymptomatic infectionsrangefrom55to75%.12,14–16Thefirstreportsofunusual
epidemics of ‘‘pain, skin eruption and general manifestations’’ thoughttohavebeenduetoRRVoccurredin1928inNewSouth Wales,Australia.17,18AlargeRRVoutbreakoccurredinthePacific
in 1979-1980 withover 500.000cases reported,16and affected
severalPICTsincludingFiji,CookIslands,AmericanSamoa,New Caledonia,Wallis&Futuna,andVanuatu.14,19–23InFP,duetothe
neighbouringRRVepidemics,patientspresentingwitha‘‘dengue likesyndrome’’wereroutinelytestedforRRVinadditiontoDENV betweenAprilandAugust1980thensporadicallyuntilFebruary 1984.AlthoughnoRRVinfectionwasdetectedduringthisperiod
ARTICLE INFO Articlehistory: Received6May2015
Receivedinrevisedform6June2015 Accepted9June2015
CorrespondingEditor:EskildPetersen, Aarhus,Denmark Keywords: RossRiver FrenchPolynesia Seroprevalence Blooddonors SUMMARY
Objectives:RossRiverisanemergingmosquito-bornediseaseintheWesternPacific.RossRivervirus (RRV)circulationhasbeensporadicallyreportedinsomePacificIslandCountriesandTerritoriesbut neverinFrenchPolynesia.TodetermineifRRVhascirculatedlocallyamongtheFrenchPolynesian population,weconductedaseroprevalencestudyonblooddonors.
Methods:Seraof593blooddonorswerecollectedfromJuly2011toOctober2013andtestedbyELISAfor thepresenceofRRV-specificImmunoglobulinG(IgG)antibodies.
Results:Atotalof204(34.40%)blooddonorswerefoundseropositiveforRRV.Amongthe132blood donorsthatwereborninFrenchPolynesiaandhadnevertravelledabroad,56(42.42%)hadRRV-specific IgGs.
Discussion: OurresultssupporttheexistenceofautochthonousRRVtransmissionandsuggestthatthis pathogen hassilentlycirculated inFrenchPolynesia.Thesefindingsraisethequestionof possible undetectedcirculationofRRVinotherPacificIslandCountriesandTerritories.
ß2015TheAuthors.PublishedbyElsevierLtdonbehalfofInternationalSocietyforInfectiousDiseases. ThisisanopenaccessarticleundertheCCBY-NC-NDlicense( http://creativecommons.org/licenses/by-nc-nd/4.0/).
* Corresponding author: Maite Aubry, Institut Louis Malarde´, PO BOX 30, 98713Papeete,Tahiti,FrenchPolynesia.
Tel./fax:+68940416460/(689)40431590. E-mailaddress:maubry@ilm.pf(M.Aubry).
ContentslistsavailableatScienceDirect
International
Journal
of
Infectious
Diseases
j o urn a l hom e pa ge : ww w. e l s e v i e r. c om/ l o ca t e / i j i d
http://dx.doi.org/10.1016/j.ijid.2015.06.005
1201-9712/ß2015TheAuthors.PublishedbyElsevierLtdonbehalfofInternationalSocietyforInfectiousDiseases.ThisisanopenaccessarticleundertheCCBY-NC-ND license(http://creativecommons.org/licenses/by-nc-nd/4.0/).
(unpublisheddata),circulationofRRVinFPcannotbeexcluded. Afterthe1979-1980outbreak,RRVapparentlydisappearedfrom thePICTs.However, casesof RRVinfections weresubsequently reportedfromtravelersreturningfromFiji:2Canadiantravelers, respectivelyin 2003 and 2004,24 and 5 NewZealand travelers, respectivelyin1997,2000,2001,2003and2009.16EvidenceofRRV
infections were also found among residents of Papua New Guinea.25
Todate,fewdataareavailableaboutthecirculation,incidence and prevalence of RRV in the Pacific. To our knowledge, 13serosurveyshavebeenconductedforRRVintheregion.12,14,20
AmongthestudiesperformedinAustralia,12seropositivityranged
from8%for seracollected in North and Southeast Queensland, DarwinandNorthernterritoryareain1974-197526toupto55%for
seracollectedfromaboriginalcommunitiesinNorthQueensland andNorthernterritoryin1966-1971.27Inaserosurveyconducted
byTeshetal.inseveralPICTs,28evidenceofRRVinfectionswas
foundamongpopulationssampledinPapuaNewGuineabetween 1960and1969andinSolomonIslandsbetween 1960and1966, withratesofRRVseropositivityamonglocalitiesrangingfrom10% to64%and1%to17%,respectively.Incontrast,noRRVantibodies werefoundinseracollectedinVanuatuin1963and1972,New Caledoniain1963,Palauin1961and1974,andAmericanSamoain 1962.InastudyfurtherconductedinAmericanSamoa,43.8%ofthe peoplesampledat theend ofthe1979-1980RRVoutbreakhad evidenceofRRVinfection,whereasthosepreviouslysampledin 1972hadnoRRVantibodies.20InFiji,seroprevalencewasover90%
insomecommunitiesaftertheRRVoutbreakin1979-1980.14In theonlystudyconductedamongblooddonors,seroprevalencefor RRVantibodieswas8.4%fromthe2,952seracollectedinSouth Australiain1992.29Toourknowledge,exceptforAustraliawhere RRVisthemostcommonandwidespreadarboviraldiseasewith about5,000casesnotifiedannually,11,30andtoalesserextentfor
Fiji,16,24therearenorecentdataaboutcirculationofRRVinthe
Pacificarea.
DuetotheincidenceofRRVinfectionsinAustraliaandfrequent population movements across the Pacific region, the risk of emergenceofthisvirusinPICTs,ashappenedintheearly80s,14,19– 23ishigh.Morerecently,thedetectionofsporadiccasesofRRV
infectionsfromFiji16,24showsthatthispathogenremainsaserious
threattothePICTs.InordertodetermineifRRVhasalreadybeen
introducedandhascirculatedinFP,weconductedaserological survey on 593 blood donors sera collected from July 2011 to October2013.
2. MaterialsandMethods 2.1. Participants
BlooddonorswererecruitedbytheFrenchPolynesianblood bankcentre(Tahiti,FP).AllblooddonorslivedinTahiti,themost inhabitedislandofFP,andwereover18yearsold.Writtenconsent fortheuseofaserumsampleforserologicaltestingwasobtained beforeblood collectionforalltheblooddonorsincludedinthis study. Volunteers to blood donation reporting a ‘‘dengue like syndrome’’in thepast3 months,oranysymptoms ofacute or recentinfection,wereexcludedfromblooddonation.Noneofthe blooddonorshasbeensampledspecificallyforthepurposeofthis study.Amedicalquestionnairewascompletedbythephysicianof thebloodbankcenterbeforebloodcollection,inaccordancewith therecommendationsforblooddonation.Thenumberofyearsof residencein FP and the pasthistory of travel outside FP were recordedforallblooddonors.
Atotalof593blooddonorsrecruitedfromJuly2011toOctober 2013wereincludedinthis study.Basedon theirtravelhistory, blooddonorsweredividedinto3groups:group1iscomposedof residentswhowereborninFPand havenevertravelledabroad (132blooddonors);group2ofresidentswhowereborninFPand havetravelledatleastonceabroad(290blooddonors);andgroup 3ofimmigrants(171blooddonors).Withingroups2and3,blood donorsreportingpasttravelincountrieswithorwithoutreported RRV autochthonous infections (Figure 1) were separated in 2subgroups,aandbrespectively(Table1).
2.2. SampleCollection
Blood samples for serological testing were collected in BD Vacutainer1 Blood Collection tubes and stored at + 48C for maximum1dayatthebloodbankcentrebeforeshipmenttothe ‘‘InstitutLouisMalarde´’’(ILM),Tahiti,FP.AtILM,bloodsamples were centrifuged for 15minutes at 1,300g then sera were retrievedandfrozenat–208Cuntilprocessing.
Figure1.CirculationofRossrivervirusinthePacific.CountrieswithreportedRossRivervirusautochthonousinfectionsarecircledinred.FrenchPolynesiaiscircledinblue. M.Aubryetal./InternationalJournalofInfectiousDiseases37(2015)19–24
2.3. ProductionofrecombinantantigensfromRRVandCHIKV Serumsamplesweretestedforthepresenceofimmunoglobulin G class antibodies (IgGs) against RRV by indirect ELISA using recombinantantigensfromRRV.GiventhatCHIKVhascirculated in the PICTs since 2011 and is antigenically related to RRV, recombinantantigensfromCHIKVwerealsousedtotestserum samples.
Recombinantantigens were produced in Drosophila S2 cells using the Drosophila S2 expression system (Life Technologies, USA).Thesyntheticgenes(GeneCust,Luxembourg)encodingthe solubleectodomain oftheenvelopeE2 glycoprotein(sE2) from RRVstrainQML1(GenBankaccessionno.GQ433354)orCHIKVLa Reunion strain06-49 (GenBankaccessionno. AM258994) were clonedintotheshuttlevectorpMT/BiP/HisAinwhichthe SNAP-tag sequence (Covalys Biosciences AG, Switzerland) had been initiallyinsertedasastabilizingprotein.Theresultingplasmids encodingeither thechimericproteinRR.sE2-SNAPor CHIK.sE2-SNAPweretransfectedintoS2cellstoestablishstablecelllinesS2/ RR.sE2-SNAP,andS2/CHIK.sE2,31accordingtothemanufacturer’s
recommendations (Life Technologies, USA). After a 10-days cadmiuminduction of thestable S2cell lines grownin 1-Liter spinner, cellsupernatants wererecoveredand secreted soluble His-taggedrecombinantviralantigenswerepurifiedonchelating andsize-exclusionchromatographycolumns.Theproteinamounts ofhighly purified RR.sE2-SNAPand CHIK.sE2-SNAPwere deter-mined using a BCA protein assay kit (Thermo Scientific, USA), accordingtomanufacturer’sinstructions.Atleast50mgofeach recombinantviralantigen(concentration:0.5to1mg/ml) were obtainedfromasinglebatchof1-LofS2cellculture.Thesamples ofpurifiedRR.sE2-SNAPandCHIK.sE2-SNAPproteinswerekeptat -808C.
2.4. ProtocolofindirectELISA
Forthecaptureofanti-RRVandanti-CHIKVIgGs,RR.sE2-SNAP, CHIK.sE2-SNAP,and antigencontrol(SNAP)weredilutedat the finalconcentration of2
m
g/mL in phosphatebuffersaline(PBS, Biome´rieux,France),and100m
Lofproteinsamplewerecoatedin 96-wellplatesovernightat+48C.Afterincubation,antigensample wasremovedandwellswereblockedwithPBScontaining3%of skimmedmilk(Re´gilait,France)and1%ofsodiumazide(Merck, Germany).Sera ofparticipants,aswellasnegativeandpositive controlsera,werediluted1:400in PBSwith3% skimmedmilk, 0.05%Tween20and1%sodiumazide.Then,eachdilutedserum was added in 2 wells containing either RR.sE2 or CHIK.sE2 recombinant antigens, and in 2 wells containing only SNAP proteins. Plates were incubated for 1 hour at 418C andsubsequently washed using PBS with 0.05% Tween 20 (Merck, Germany).Peroxidase-conjugatedgoatanti-humanIgGantibodies (Jackson ImmunoResearch, USA) were added in all wells at a dilutionof1:10000inPBSwith3%skimmedmilkand0.05%Tween 20.Plateswereincubatedfor1hourat418Candwashedbefore additionofperoxidasesubstratetetramethylbenzidine(TMB,KPL, USA). Plates werestored at room temperature in the dark for 5minutesandtheenzymaticreactionbetweentheperoxidaseand itssubstratewasstoppedbytheadditionof TMBStopSolution (KPL,USA).Theabsorbancewasreadatawavelengthof450nm (OD450)usingamicroplatephotometer(ThermoScientific,USA).
SerafoundpositiveforRRVIgGsusingrecombinantsantigens werealsotestedusingthekitPanbioRossRiverVirusIgGELISA (Panbiodiagnostics,USA),followingmanufacturer’s recommenda-tions.
2.5. Serologicalanalysis
Foreachserum,averageabsorbancewascalculatedusingthe OD450 values measured in the 2 wells containing the same
recombinant antigenorSNAPproteins.Specificabsorbancewas then determined by deducting the mean absorbance value obtainedwithSNAPtothemeanabsorbancevaluefoundforeach recombinant antigen. Sera with a specific absorbance value 0.2wereconsideredpositiveforthepresenceofIgGsagainstthe virustested.
2.6. Statisticalanalysis
To assess the impact of age and travel history on RRV seroprevalence among participants,Fisher’s testwasperformed usingtheGraphPadPrism6version6.03software.Pvalues less than0.05wereconsideredasstatisticallysignificant.
2.7. EthicsStatement
The recruitment of participants and processing of blood sampleswereconductedinaccordancewiththeEthicsCommittee of French Polynesia under reference n860/CEPF (06/27/2013). Blood sample and personal data of each participant were anonymizedat theFrenchPolynesianblood bankcentre before sendingtoILM.
3. Results
Amongthe593blooddonors,204(34.40%),18(3.03%)and10 (1.69%)werefoundseropositivefor RRV,CHIKVorbothviruses IgGs,respectively(Table2).Seroprevalenceindifferentgroupsand
Table1
Characteristicsoftheblooddonorsincludedinthestudy
Blooddonors BorninFP Immigrants Total
Group1 Group2a Group2b Totalgroup2 Group3a Group3b Totalgroup3
Number 132 145 145 290 101 70 171 593 % 22.26 24.45 24.45 48.90 17.03 11.80 28.84 100 Age Range 18-59 18-69 18-63 18-69 19-75 19-72 19-75 18-75 Mean 32.80 38.13 31.93 35.03 44.78 41.11 43.28 36.91 Median 32.00 37.00 29.00 33.00 46.00 41.00 42.00 36.00 YearsofresidenceinFP Range 18-59 12-69 15-63 12-69 0-49 0-50 0-50 0-69 Mean 32.80 37.47 31.65 34.56 17.16 11.41 14.81 28.47 Median 32.00 36.00 29.00 32.00 16.00 7.50 12.00 27.00 Group1:residentswhowereborninFPandhavenevertravelledabroad;group2a:residentswhowereborninFPandhavetravelledatleastonceinacountrywithreported RRVinfections;group2b:residentswhowereborninFPandhavetravelledatleastoncebutincountrieswithoutreportedRRVinfections;group3a:immigrantswhohave travelledatleastonceinacountrywithreportedRRVinfections;group3b:immigrantswhohavetravelledatleastoncebutincountrieswithoutreportedRRVinfections.
subgroupsrangedfrom21.43%(group3b)to42.42%(group1)for RRVand it rangedfrom0%(group 3b) to5.94% (group 3a) for CHIKV.Percentages ofRRVseropositivitywerenot significantly differentbetweengroupsexceptforgroup3bagainstgroups1and 2b(Pvalues were0.0032and 0.0408,respectively).Among the 204blooddonorsseropositiveforRRVIgGs,14werealsofound positiveusingthekitPanbioRossRiverVirusIgGELISA.
Seroprevalence forRRVaccordingtotheyearofbirthor the lengthofstayinFPofblooddonorsthathavenevertravelledin areaswithknowncirculationofRRVisreportedinTable3.Among blooddonorsbornafter1981belongingtogroups1and2b,37.09% and 31.16%wereseropositive for RRV, respectively. In thetwo groups, therate of positivity for RRV IgGsincreased with age. Amongblooddonors ofgroup3b whoarrivedin FPduring the years1982-2000,2001-2005and2006-2013,40%,25%and5.88% wereseropositiveforRRV,respectively.
4. Discussion
ArbovirusesareemergingpathogensinOceania8,32and,except
forDENV,fewdataareavailableabouttheircirculation,incidence andprevalenceintheregion.Inparticular,thespreadofRRVinthe Pacificregionisunknown.Inthepresentstudy,samplecollection wasconductedinFPfromJuly2011toearlyOctober2013.Evenif thefirst CHIKV outbreak in FP was recorded in October 2014, CHIKV had begun circulating in other PICTs from 2011.8
Consequently,aprevioussilentcirculationofCHIKVinFPcannot beexcluded.ToinsurethatthedetectionofRRVIgGswasnotdue to cross-reaction of RRV recombinant antigens with CHIKV antibodiesresultingfroma non-detected previous infection,all seraweretestedforthepresenceofCHIKVIgGs,inadditiontoRRV IgGs. The low rate of immunization against CHIKV measured among blood donors (3.03%) suggests that the virus did not
activelycirculateinFPbefore2014.Thishypothesisissupported by the large magnitude of theCHIKV outbreak that started in October 2014,withatleast 25%ofthepopulation estimatedto havebeeninfected.33Moreover,thesmallnumberofserafound
positive for both RRV and CHIKV IgGs (10/593) suggests the absenceorlimitedcross-reactionsbetweenthetwoAlphaviruses withourELISAassay.
The204serafoundpositiveforRRVIgGsusing recombinant antigenswerealsotestedwithacommercialserologicalassay(kit PanbioRossRiverVirusIgGELISA),and14(6.86%)ofthemwere foundpositivewithbothassays,confirmingthecirculationofRRV in FP. Discordant results between in-house and commercial serologicaltestshavealreadybeenreportedforotherarboviruses. Forinstance,twocommercialELISAkitsevaluatedforthedetection ofCHIKVIgGsinserumsamplespreviouslytestedpositivewith in-houseELISAsfrom2NationalReferenceCentersforArboviruses showedsensitivitiesof52%and88%.34Moreover,whencomparing
the performance of several serological tests for detecting JEV-specificIgGsin29vaccinatedchildren,thein-houseassaydetected neutralizing antibodies in all children whereas thecommercial ELISA assay showed no positive reaction.35 In another study
conductedonserumsamplesfrom100personsvaccinatedagainst JEV,only6.6%oftheserafoundpositivewiththein-houseassay werealsodetectedpositiveusingacommercialIgGELISAtest.36 Thediscrepancybetweentheresultsobtainedwithlaboratoryand commercial assays may be related to the cut-off used. For a diagnosispurpose (commercial kit),thecut-off is highbecause specificityispreferredtosensitivity.Moreover,diagnostickitsare dedicatedtothedetectionofrecentratherthanpastinfectionsand should not beused toscreen general population, which is the purpose of seroprevalence studies. According to the manufac-turer’sprotocol,thecut-offofthecommercialkitusedinourstudy was determined on an Australian population and may require
Table2
SeropositivityforRRVandCHIKVineachgroupofblooddonors
Blooddonors BorninFP Immigrants Total
Group1 Group2a Group2b Totalgroup2 Group3a Group3b Totalgroup3 SeropositiveforRRV
Total 56(2)a
49(6) 52(5) 101(11) 32(1) 15(0) 47(1) 204(14) % 42.42 33.79 35.86 34.83 31.68 21.43 27.48 34.40 SeropositiveforCHIKV
Total 2 6 4 10 6 0 6 18
% 1.51 4.14 2.76 3.45 5.94 0 3.51 3.03
SeropositiveforbothRRVandCHIKV
Total 1 4 3 7 2 0 2 10
% 0.76 2.76 2.07 2.41 1.98 0.00 1.17 1.69
a
NumberofblooddonorstestedpositiveforRRVwiththekitPanbioRossRiverVirusIgGElisa.
Table3
SeropositivityforRRVaccordingtotheyearofbirthorthenumberofyearsofresidenceforblooddonorsthathavenevertravelledincountrieswithreportedRRVinfections BlooddonorsseropositiveforRRV Group1 Group2b Group3b BorninFP
Bornbefore1981 33/70(47.14%) 28/68(41.17%) – Bornfrom1982to1987 8/20(40.00%) 12/37(32.43%) – Bornfrom1988to1992 10/27(37.03%) 10/31(32.25%) – Bornafter1993 5/15(33.33%) 2/9(22.22%) – Totalbornafter1981 23/62(37.09%) 24/77(31.16%) – Totalbornbeforeandafter1981 56/132(42.42%) 52/145(35.86%) – Immigrants
ArrivedinFPbefore1981 – – 3/8(37.5%)
ArrivedinFPbetween1982-2000 – – 8/20(40.00%) ArrivedinFPbetween2001-2005 – – 2/8(25.00%) ArrivedinFPbetween2006-2013 – – 2/34(5.88%) TotalarrivedinFPafter1981 – – 12/62(19.35%) TotalarrivedinFPbeforeandafter1981 – – 15/70(21.43%)
M.Aubryetal./InternationalJournalofInfectiousDiseases37(2015)19–24 22
adjustmentdependingonthepopulationanalyzed.Consequently, thecut-off of the commercial assay shouldbe adapted for the analysis of the serological results obtained from the French Polynesianpopulation.
TheoverallrateofRRVseropositiveblooddonorsfoundinour studywassurprisinglyhigh(34.40%)giventhatRRVinfectioncases hadneverbeenreportedinFP.Theabsenceofsignificantdifference inprevalencebetweenblooddonorswhowereborninFPandhave travelledornotinareaswithorwithoutRRVreportedinfections (groups1and2),suggeststhattheyhavebeeninfectedinFP.The highratesofRRVseropositivityfoundamongblooddonorswho werebornin FPafter 1981,whatevertheyhad never travelled abroad(group1,37.09%)orhadtravelledonlyinareaswithout RRVreportedcases(group2b,31.16%),supporttheideathatRRV hascirculatedinFPafterthelargeoutbreakthatoccurredin 1979-1980inthePICTs.Thelowest(21.43%)andhighest(42.42%)RRV seroprevalencerates arefoundfor theimmigrantgroupthat is supposednottohavebeenexposedelsewherethaninFP(group 3b)andforthegroupofresidentswhowereborninFPandhave nevertravelledabroad(group1),respectively,andaresignificantly differentbetweenthetwogroups(P=0.0032).Togetherwiththe mediantime ofresidencein FPfor theimmigrants(7.50years) whichis4timeslowerthantheonefoundfortheblooddonors borninFP(32.00years),thesedatasuggestthattheincreaseinRRV seroprevalenceislinkedtothetimeofresidenceinFP.Theincrease withageoftheacquisitionofRRVIgGsamongtheresidentsbornin FPandthatcouldhavebeeninfectedonlylocally(goups1and2b) isconsistentwithasilentcontinuouscirculationofRRVduringthe last decades. This is confirmed by the detection of 12 RRV seropositiveblooddonors amongimmigrantswhoarrivedinFP between 1982-2013and whohave nevertravelledin countries withreportedRRVinfections(group3b).ThefindingthatRRVhas circulated in FP is concordant with the presence of several mosquitospeciesthatcanpotentiallytransmitthevirus,including Aedes aegypti, Aedes polynesiensis, Culex annulirostris, Culex quinquefasciatusandCulexsitiens.12,19,37–41
RRV may have circulated in FP without being detected for severalreasons.Themainoneisthat55%to75%ofRRVinfections areasymptomatic,12,14–16and manysymptomatic patientshave
mildsymptomsthatmaynotrequiretoseekmedicalattention.In addition,RRVinfectionscanhaveclinicalpresentationssimilarto DENV infections. However, withlaboratory capacities for arbo-virusesdetection mainlyfocused on DENV, patients presenting witha‘‘denguelikesyndrome’’buttestednegativeforDENVare notsystematicallyinvestigatedforotherarboviruses.Atlast,virus isolationisrarelyachieved,probablybecauseRRVdoesnotpersist beyond the early stages of disease,12 which may explain why despite laboratory diagnosis, no RRV infectious cases were detectedinFPbetween1980-1984.
Onlyadultsweretestedinthisstudybutsincemostinfections occurbetween theagesof 20and 60,peaking between30 and 40,16,42 it should be relevant. Thus, despite the exclusion of
childrenanddiscrepantresultsinthepercentageofRRVpositive blooddonorsdependingonserologicalmethodologyused,wecan concludetoasilentcirculationofRRVinFP.Irrefutableevidenceof autochthonousRRVtransmissioninFPwouldrequiretheisolation ofthevirusorofitsRNAfromaresidentwithnorecenttravel history. AttemptstoisolateRRVwillbeperformed in a second studyonseracollectedfrompatientspresentingwithsymptoms suggestiveofanarbovirusinfectionandtestednegativeforDENV, ZIKVandCHIKV.
LikeRRV,it ispossiblethatotherarboviruses mayalsohave circulatedinFPandinotherPICTswithoutbeingdetected.Indeed, theoccurrenceofWestNilevirusorJEVintroductionsrespectively fromtheUSAandJapanarepossiblesincemanyPICTshavedirect andfrequentflightsfromthesecountries,and severalmosquito
speciesestablishedinthePICTsmaytransmittheseviruses.38Due
tothegrowingriskofemergenceofnewarbovirusesinthePacific, joint efforts should be done to improve local and regional surveillance,43aswellasvectorcontrol.
Acknowledgments
We are grateful to Je´roˆme Viallon from the Institut Louis Malarde´,FrenchPolynesia,fortechnicalsupport,andtoPhilippe BuchyfromtheInstitutPasteurinCambodia,forprovidingCHIKV positivecontrolserum.
This study wassupported by the ‘‘Contrat deprojets 2012-2014’’(ConventionNo.7331/MSS/DSP,08/31/2012).
Conflict of interest statement: None of the authors have any conflictofinterest(financialorpersonal)inthisstudy.
Ethical approval statement: This study was approved by the EthicsCommitteeofFrenchPolynesiaunderreferencen860/CEPF (06/27/2013).
References
1.SinghN,KiedrzynskiT,LepersC,BenyonEK.DengueinthePacific–anupdateof thecurrentsituation.PacHealthDialog2005;12(2):111–9.
2.DesclouxE,Cao-LormeauVM,RocheC,DeLamballerieX.Dengue1diversity andmicroevolution,FrenchPolynesia2001-2006:connectionwith epidemiol-ogyandclinics.PLoSNeglTropDis2009;3(8):e493.
3.Cao-LormeauVM,RocheC,AubryM,TeissierA,LastereS,DaudensE,etal. Recentemergenceofdenguevirusserotype4inFrenchPolynesiaresultsfrom multipleintroductionsfromotherSouthPacificIslands.PLoSOne2011;6(12): e29555.
4.Cao-LormeauVM,RocheC,MussoD,MalletH-P,DalipandaT,DofaiA,etal. Dengue virus type 3, South pacific islands, 2013. Emerg Infect Dis 2014;20(6):1034–6.
5.Cao-LormeauVM,RocheC,TeissierA,RobinE,BerryA-L,MalletH-P,etal.Zika virus, French polynesia, Southpacific, 2013. EmergInfect Dis2014;20(6): 1085–6.
6.MussoD,NillesEJ,Cao-LormeauVM.RapidspreadofemergingZikavirusinthe Pacificarea.ClinMicrobiolInfect2014;20(10).O595-6.
7.AubryM,TeissierA,RocheC,RichardV,ShanYanA,ZisouK,etal.Chikungunya outbreak,FrenchPolynesia,October2014.EmergInfectDis2015;21(4):724–6.
8.Cao-Lormeau VM, Musso D. Emerging arboviruses in the Pacific. Lancet 2014;384(9954):1571–2.
9.DuffyMR,ChenT-H,HancockWT,PowersAM,KoolJL,LanciottiRS,etal.Zika virusoutbreakonYapIsland,FederatedStatesofMicronesia.NEnglJMed 2009;360(24):2536–43.
10.BaigS,FoxK,JeeY,O’ConnorP,HombachJ,WangS,etal.JapaneseEncephalitis SurveillanceandImmunization—AsiaandtheWesternPacific,2012.Morb MortalWklyRep2013;62(33):658–62.
11.Barber B, Denholm JT, SpelmanD. Ross River virus. Aust Fam Physician 2009;38(8):586–9.
12.HarleyD,SleighA,RitchieS.RossRiverVirusTransmission,Infection,and Disease:aCross-DisciplinaryReview.ClinMicrobiolRev2001;14(4):909–32.
13.DohertyRL,WhiteheadRH,GormanBM,O’GowerAK.Theisolationofathird groupAarbovirusinAustraliawithpreliminaryobservationsonitsrelationship toepidemicpolyarthritis.AustJSci1963;26:183–4.
14.AaskovJG,MataikaJU,LawrenceGW,RabukawaqaV,TuckerMM,MilesJA,etal. AnepidemicofRossRivervirusinfectioninFiji,1979.AmJTropMedHyg 1981;30(5):1053–9.
15.RussellRC,CopeSE,YundAJ,HuestonL.Combattingtheenemy-mosquitoes andRossRivervirusinajointmilitaryexerciseintropicalAustralia.AmJTrop MedHyg1998;59:S307.
16.LauC,WeinsteinP,SlaneyD.ImportedcasesofRossRivervirusdiseaseinNew Zealand-atravel medicineperspective.TravelMedInfectDis2012;10(3): 129–34.
17.EdwardsA.Anunusualepidemic.MedJAust1928;1:664–5.
18.NimmoJ.Anunusualepidemic.MedJAust1928;1:549–50.
19.Rosen L, GublerDJ,BennettPH. Epidemicpolyarthritis(Ross River) virus infectionintheCookIslands.AmJTropMedHyg1981;30(6):1294–302.
20.Tesh RB, McLean RG,ShroyerDA, CalisherCH,Rosen L. RossRivervirus (Togaviridae: Alphavirus) infection (epidemic polyarthritis) in American Samoa.TransRSocTropMedHyg1981;75(3):426–31.
21.PanonG,LeGonidecG,FauranP.Laboratorydiagnosisofepidemicpolyarthritis (RossRivervirus)inNewCaledonia.BullSocPatholExotFiliales1983;76(5Pt 2):755–60.
22.FauranP,LeGonidecG,RodhainF.ResearchonviralinfectionsinSouthPacific mosquitoesundernaturalconditions.BullSocPatholExotFiliales1984;77(5): 628–36.
23.FauranP,DonaldsonM,HarperJ,OseniRA,AaskovJG.CharacterizationofRoss RivervirusesisolatedfrompatientswithpolyarthritisinNewCaledoniaand WallisandFutunaIslands.AmJTropMedHyg1984;33(6):1228–31.
24.KlapsingP,MacLeanJD,GlazeS,McCleanKL,DrebotMA,LanciottiRS,etal.Ross Rivervirusdiseasereemergence,Fiji,2003–2004.EmergInfectDis2005;11(4): 613–5.
25.HiiJ,DykeT,DagoroH,SandersRC.Healthimpactassessmentsofmalariaand RossRivervirusinfectionintheSouthernHighlandsProvinceofPapuaNew Guinea.PNGMedJ1997;40(1):14–25.
26.StallmanND,WiemersMA,BourkeAT.Serologyindiagnosisandsurveysof man.ArbovirusResAust1976;1:46–64.
27.DohertyRL,GormanBM,WhiteheadRH,CarleyJG.Studiesofepidemic poly-arthritis:thesignificanceofthreegroupAarbovirusesisolatedfrom mosqui-toesinQueensland.AustralasAnnMed1964;13:322–7.
28.TeshRB,GajdusekDC,GarrutoRM,CrossJH,RosenL.Thedistributionand prevalenceofgroupAarbovirusneutralizingantibodiesamonghuman popula-tionsinSoutheastAsiaandthePacificislands.AmJTropMedHyg1975;24(4): 664–75.
29.Weinstein P,Worswick D, MacintyreA,Cameron S.Human sentinelsfor arbovirussurveillanceandregionalriskclassificationinSouthAustralia.Med JAust1994;160(8):494–9.
30.YuW,MengersenK,DaleP,MackenzieJS,TolooGS,WangX,etal. Epidemio-logicpatternsofRossRivervirusdiseaseinQueensland,Australia,2001–2011. AmJTropMedHyg2014;91(1):109–18.
31.WarterL,LeeCY,ThiagarajanR,GrandadamM,LebecqueS,LinRTP,etal. Chikungunya virus envelope-specific human monoclonal antibodies with broadneutralizationpotency.JImmunol2011;186(5):3258–64.
32.KlineK,McCarthyJS,PearsonM,LoukasA,HotezPJ.Neglectedtropicaldiseases of Oceania:reviewoftheirprevalence,distribution,andopportunitiesfor control.PLoSNeglTropDis2013;7(1):e1755.
33.NhanTX,MussoD.TheburdenofchikungunyainthePacific.ClinMicrobiol Infect2015.
34.PratCM,FlusinO,PanellaA,TenebrayB,LanciottiR,Leparc-GoffartI.Evaluation ofcommerciallyavailableserologicdiagnostictestsforchikungunyavirus. EmergInfectDis2014;20(12):2129–32.
35.ChaGW,ChoJE,JuYR,HongY-J,HanMG,LeeW-J,etal.Comparisonof fourserologicaltestsfordetectingantibodiestoJapaneseencephalitisvirus after vaccination inchildren. Osong public Heal Res Perspect 2014;5(5): 286–91.
36.LitzbaN,KladeCS,LedererS,NiedrigM.Evaluationofserologicaldiagnostictest systemsassessingtheimmuneresponsetoJapaneseencephalitisvaccination. PLoSNeglTropDis2010;4(11):e883.
37.GublerDJ.TransmissionofRossRivervirusbyAedespolynesiensisandAedes aegypti.AmJTropMedHyg1981;30(6):1303–6.
38.GuillaumotL.ArbovirusesandtheirvectorsinthePacific-Statusreport.Pac HealDialog2005;12(2):45–52.
39.LardeuxFJ.BiologicalcontrolofCulicidae with thecopepodMesocyclops aspericornisandlarvivorousfish(Poeciliidae)inavillageofFrenchPolynesia. MedVetEntomol1992;6(1):9–15.
40.MercerDR,BossinH,SangMC,O’ConnorL,DobsonSL.Monitoringtemporal abundanceandspatialdistributionofAedespolynesiensisusingBG-Sentinel trapsinneighboringhabitatsonRaiatea,SocietyArchipelago,FrenchPolynesia. JMedEntomol2012;49(1):51–60.
41.RageauJ.Inventairedesarthropodesd’inte´reˆtme´dicaletve´te´rinairedansles territoiresfranc¸aisduPacifiquesud.MedVetEntomol1958;3:873–82.
42.RussellRC,DwyerDE.ArbovirusesassociatedwithhumandiseaseinAustralia. MicrobesInfect2000;2(14):1693–704.
43.DerraikJGB,SlaneyD,NyeER,WeinsteinP.Vector-bornedisease preven-tion:theneedforajointSouthPacificapproach.NZMedJ2009;122(1299): 7–12.
M.Aubryetal./InternationalJournalofInfectiousDiseases37(2015)19–24 24