Low chikungunya virus seroprevalence two years after emergence in Fiji

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Low chikungunya virus seroprevalence two years after

emergence in Fiji

Maïté Aubry, Mike Kama, Alasdair Henderson, Anita Teissier, Jessica

Vanhomwegen, Teheipuaura Mariteragi-Helle, Tuterarii Paoaafaite,

Jean-Claude Manuguerra, Ketan Christi, Conall Watson, et al.

To cite this version:

Maïté Aubry, Mike Kama, Alasdair Henderson, Anita Teissier, Jessica Vanhomwegen, et al.. Low

chikungunya virus seroprevalence two years after emergence in Fiji. International Journal of Infectious

Diseases, Elsevier, 2020, 90, pp.223-225. �10.1016/j.ijid.2019.10.040�. �pasteur-02875151�

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Short

Communication

Low

chikungunya

virus

seroprevalence

two

years

after

emergence

in

Fiji

Maite

Aubry

a,

*

,

Mike

Kama

b,c

,

Alasdair

D. Henderson

d

,

Anita

Teissier

a

,

Jessica

Vanhomwegen

e

,

Teheipuaura

Mariteragi-Helle

a

,

Tuterarii

Paoaafaite

a

,

Jean-Claude

Manuguerra

e

,

Ketan

Christi

c

,

Conall

H. Watson

d,f

,

Colleen

L. Lau

g

,

Adam

J. Kucharski

d

,

Van-Mai

Cao-Lormeau

a

InstitutLouisMalardé,POBOX30,98713Papeete,Tahiti,FrenchPolynesia

b

FijiCentreforCommunicableDiseaseControl,TamavuaHospitalComplex,MataikaHouse,Suva,Fiji

c_The_University_of_the_South_Paciﬁc,_Private_Mail_Bag,_Laucala_Campus,_Suva,_Fiji d

LondonSchoolofHygieneandTropicalMedicine,KeppelStreet,LondonWC1E7HT,UnitedKingdom

e

InstitutPasteur,25-28,rueduDocteurRoux75724ParisCedex15,France

f

EpidemicResearchGroupOxford,UniversityofOxford,OxfordOX37BN,UnitedKingdom

g

ResearchSchoolofPopulationHealth,TheAustralianNationalUniversity,62MillsRoad,Acton,ACT2601,Australia

ARTICLE INFO Articlehistory: Received11July2019

Receivedinrevisedform28October2019 Accepted30October2019 Keywords: Chikungunya RossRiver Arbovirus Seroprevalence Fiji Paciﬁc ABSTRACT

Objectives:InFiji,autochthonouschikungunyavirus(CHIKV)infectionwasﬁrstdetectedinMarch2015. In a previousserosurveyconductedduring October–November 2015, we reportedaprevalence of anti-CHIKVIgGantibodiesof0.9%.Inthepresentstudy,weinvestigatedtheseroprevalenceofCHIKV twoyearsafteritsemergenceinFiji.

Methods:Serafrom320residentsofFijirecruitedinJune2017,fromthesamecohortofindividualsthat participatedintheserosurveyin2015,weretestedforthepresenceofIgGantibodiesagainstCHIKVusing arecombinantantigen-basedmicrosphereimmunoassay.

Results:Between2015and2017,CHIKVseroprevalenceamongresidentsincreasedfrom0.9%(3/333)to 12.8%(41/320).Oftheparticipantswithavailable serumsamplescollected inboth2015and2017 (n=200),31(15.5%)whowereseronegativein2015hadseroconvertedtoCHIKVin2017.

Conclusions:Ourﬁndingssuggestthatlow-leveltransmissionofCHIKVoccurredduringthetwoyears followingtheemergenceofthe virus in Fiji.No CHIKVinfection has been reportedin Fiji since 2017, butdue to thepresumedlowherdimmunityofthepopulation,theriskofCHIKVre-emergenceishigh.Consequently, chikungunyashouldbeconsideredinthedifferentialdiagnosisofacutefebrilediseasesinFiji.

Introduction

Chikungunya virus (CHIKV, Alphavirus genus, Togaviridae family) is transmitted to humans by Aedes mosquitoes. CHIKV infection causes an acute febrile illness commonly with poly-arthralgia which can become chronic, maculopapular rash, headache, fatigueand myalgia(MinistryofHealth and Medical Services, 2015). In Fiji (884,887 inhabitants in 2017), the ﬁrst reportedCHIKVinfectionwasdetectedinMarch2015(Ministryof Healthand Medical Services,2015).FourautochthonousCHIKV infectionsweresubsequentlydetectedthesameyear,followedby

86in2016,and2in2017(Kamaetal.,2019).Duringthisperiod, CHIKVinfectionwasalsoreportedintravelersreturningfromFiji to Australia and New Zealand (The Australian Government Department ofHealth,2019;InstituteofEnvironmentalScience and Research Limited, 2018). A serosurvey conducted during October-November2015intheCentralDivision,where43%ofthe Fiji population is living, showed a prevalence of anti-CHIKV immunoglobulin class G (IgG) antibodies of 0.9% (Kama et al., 2019).Inthepresentstudy,weinvestigatedtheseroprevalenceof CHIKVinthesamepopulationtwoyearsafteremergenceinFiji. Methods

Ourstudywasconductedin320volunteerswithnosigniﬁcant acuteillnessrecruitedintheCentralDivisioninJune2017,fromthe

* Correspondingauthor.

E-mailaddress:maubry@ilm.pf(M.Aubry).

https://doi.org/10.1016/j.ijid.2019.10.040

1201-9712/©2019TheAuthors.PublishedbyElsevierLtdonbehalfofInternationalSocietyforInfectiousDiseases.ThisisanopenaccessarticleundertheCCBY-NC-ND license(http://creativecommons.org/licenses/by-nc-nd/4.0/).

InternationalJournalofInfectiousDiseases90(2020)223–225

ContentslistsavailableatScienceDirect

International

Journal

of

Infectious

Diseases

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samecohort previouslytested in 2015 (Kamaet al., 2019).All bloodsamplesweretestedforthepresenceofIgGagainstCHIKV usingthesamerecombinantantigen-basedmicrosphere immu-noassay(MIA) as in the serosurveyconducted in 2015 (Kama etal.,2019),with100%sensitivityandspeciﬁcity.Sampleswere alsotestedbyMIAforIgGagainstRossRivervirus(RRV),arelated alphavirusthatcausedalargeoutbreakinFijiin1979andhassince establishedendemiccirculation,assuggestedbyrecentevidence (Aubryetal.,2019).Asubsetofpairedserumsamplescollectedin 2015and2017 was alsotestedfor thepresenceof neutralizing antibodiesagainst CHIKVas previously described (Aubry et al., 2018).DatawereanalyzedwithGraphPadPrism6.03usingthe Fisher’sexacttest.

Results

Theprevalenceofanti-CHIKVIgGintheparticipantsfromthe CentralDivisionincreasedfrom0.9%(95%CI0.2%–2.6%)in2015to 12.8% (95%CI 9.4%–17%) in 2017 (p<0.0001) (Table 1). The prevalenceofanti-RRVIgGwasstableoverthesameperiod,with 37.2%(95%CI32.4%–42.7%)in2015and39.1%(95%CI33.7%–44.7%) in 2017 (p=0.687). Among the200 participants with available serumsamplescollectedinboth2015and2017,31(15.5%;95%CI 10.8%_–21.3%)participantswhohadnodetectableanti-CHIKVIgG and16(8%;95%CI4.6%–12.7%)withnoanti-RRVIgGin2015had seroconvertedtotheserespectivevirusesby2017(Table2).Among the31participantswithanti-CHIKVIgGin2017,5(16.1%;95%CI 5.5%–33.7%) had anti-RRV IgG in 2015. Moreover, for all 31 participants that were found seronegative in 2015 and subse-quentlytestedseropositivein2017againstCHIKVbyMIA,paired serumsampleswerealsotestedbyneutralizationassayandresults were100%concordantbetweenthetwoassays.

Discussion

AlthoughCHIKVwasintroducedtoanimmunologicallynaïve populationinFiji,asdemonstratedbyaCHIKVseroprevalence_<1% in 2015 (Kama et al., 2019), our serologicalﬁndings showthe transmissionrate inthefollowingtwoyearswasrelativelylow, withseroprevalenceof12.8%in2017.Thisresultcontrastswiththe

explosiveCHIKVoutbreakthatoccurredin2014–2015inFrench Polynesia(Aubryetal.,2015),anotherPacificislandcountry,where aseroprevalenceof76%wasfoundoneyearaftertheemergenceof thevirus(Aubryetal.,2018).Apossibleexplanationforthelarge differenceintransmissionbetweenthetwocountriesisthatrecent exposure to RRV may provide cross-protection against CHIKV infection.Indeed,higherRRVseroprevalencewasdetectedinthe general populationfrom Fiji(37.2% in 2015and 39.1% in 2017) comparedtoFrenchPolynesia(18%in2015)(Aubryetal.,2019; Aubryetal.,2017).Moreover,thefindingthat8%ofFijiresidents whowereinitiallyseronegativetoRRVhadseroconvertedbetween 2015 and 2017 suggests recent circulation of the virus in Fiji, whereasinFrenchPolynesiathelowRRVseroprevalence(1%)in children aged less than 16 years in 2014 (Aubry et al., 2017) suggestslimitedtransmissionduringthepasttwodecades.This hypothesisisfurthersupportedbyexperimentsshowingthatmice infectedwithRRVandchallengedwithCHIKV4.5monthslaterhad significantlyreducedCHIKVviremiaandwereprotectedagainst thedisease(Gardneretal.,2010).Anotherfactorthatmayhave limited circulation of CHIKV in Fiji is possible competition for transmissionbythemosquitohost(Vogelsetal.,2019),asCHIKV circulatedconcurrentlywithotherarboviruses(Zikavirus,dengue virusesand RRV) that share thesame mosquito vectors (Kama etal., 2019;Aubryet al.,2019)Additionalstudies aretherefore neededtoidentifythefactorsmodulatingconcurrenttransmission ofmultiplemosquito-bornevirusesinFiji.

Inourstudy,participantswererecruitedintheCentralDivision, where 74.2% (69/93)of theconﬁrmedcases ofCHIKV infection in Fiji were detected between 2015–2017. Serological evidence togetherwithsurveillancedata(Kamaetal.,2019)stronglysuggest low CHIKVtransmissionin Fiji between2015–2017. Since most residentsinFijiarestillsusceptibletoCHIKV,thereisahighriskof reemergence in thecomingyears. Consequently,active surveil-lanceiscrucialforearlydetectionofnewcasesofCHIKVinfection, andchikungunyashouldbeconsideredinthedifferentialdiagnosis of acute febrile illness in Fiji, particularly in the presence of polyarthralgiaand/orrash.

Funding

ThisworkwassupportedbytheFrenchministryforEuropeand Foreign Affairs [Paciﬁc Funds grant no. 04917-19/07/17]; the FrenchGovernment's “Investissementd'Avenir” Program[Labex IBEIDgrantno.ANR-10-LABX-62-IBEID];andtheWellcomeTrust [Grantno.107778/Z/15/Z].Thestudyalsoreceivedsupportfrom France and French Polynesia governments’“Contrat de Projets” [MA’I’OREprogram,grantsno.HC/372/DIE/BPT-18/05/18andno. 03298/MTF/REC-17/05/18].CHWwassupportedbytheUKMedical ResearchCouncil[grantno.MR/J003999/1]andissupportedbya UK National Institute for Health Research Epidemiology for Vaccinology [grant no. PR-OD-1017-20002]. CLL was supported byanAustralianNationalHealth and MedicalResearch Council Fellowship[grantno.1109035].ADHwassupportedbyaMedical ResearchCouncilLIDstudentship[grantno.MR/N013638/1].AJK

Table1

Prevalenceofanti-chikungunyavirusandanti-RossRivervirusantibodiesinarepresentativesubsetoftheFijianpopulationsampledintheCentralDivisionduring October-November2015(N=333)andJune2017(N=320).

Samplingperiod Agerange(median),y N No.positive(%[95%CI])

CHIKV RRV

October–November, 2015

4–80(29) 333 3(0.9[0.2–2.6]) 124(37.2[32.4–42.7])

June,2017 6–84(29) 320 41(12.8[9.4–17]) 125(39.1[33.7–44.7])

CHIKV,chikungunyavirus;RRV,RossRivervirus.

Table2

Positivityforanti-chikungunyavirusandanti-RossRivervirusantibodiesinpaired serumsamples seriallycollected fromthe sameparticipants(N=200) during October-November2015andJune2017.

2015 2017 CHIKV+ CHIKV RRV+ RRV CHIKV+ 0 2 ‒ ‒ CHIKV 31 167 ‒ ‒ RRV+ ‒ ‒ 56 12 RRV ‒ ‒ 16 116

CHIKV,chikungunyavirus;RRV,RossRivervirus.

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wassupportedbyaWellcomeTrust/RoyalSocietySirHenryDale Fellowship[grantno.206250/Z/17/Z].

Ethicalapprovalstatement

ThisstudywasapprovedbytheFijiNationalHealthResearch EthicsReviewCommittee(ref2017.20.MC)andtheLondonSchool ofHygieneand TropicalMedicineObservationalResearchEthics Committee(ref12037).

Conﬂictofintereststatement

Noneoftheauthorshaveanyconﬂictofinterest(ﬁnancialor personal)inthisstudy.

Acknowledgments

Wegreatlythankalltheparticipantsandcommunityleaders in Fijiwhogenerouslycontributedtothestudy over thethree visitsin2013,2015and2017.Wewouldliketoacknowledgethe workoftheﬁeldteams:MeredaniTaufa,AdiKuiniKadi,Jokaveti Vubaya,ColinMichel,MereaniKoroi,AtuVesikula,andJosateki Raibevu (2015); Jessica Paka, Amele Ratevono, Warren Fong, ManishaPrakash,JonetaniBola,MoseseLigani,andTainaNaivalu (2017).

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