II. THEORETICAL BACKGROUND AND PREVIOUS
1.1. The concept
DanilaB.Carvalhoa,CarlosE.Almeidaa,CláudiaS.Rochaa,SueliGardima,VagnerJ.
Mendonc¸aa,AlineR.Ribeirob,ZulimarC.P.V.T.Alvesc,KellemT.Ruellasd,
AlanVedovelid,JoãoA.daRosaa,∗
aFaculdadedeCiênciasFarmacêuticas,UNESP–Araraquara,SP,Brazil bUniversidadeEstadualdeCampinas,UNICAMP–Campinas,SP,Brazil
cSuperintendênciadeControledeEndemias(SUCEN)SR-06RibeirãoPreto,SP,Brazil dVigilânciaSanitáriaeEpidemiológica–MonteAlto,SP,Brazil
a r t i c l e i n f o
Articlehistory: Received8July2013
Receivedinrevisedform2October2013 Accepted9October2013 Available online xxx Keywords: Triatomines Domiciliation Antropogenicchanges Vectorbehavior a b s t r a c t
Afterseveralpublicnotificationsofdomiciliaryinvasions,palmtreeswereinvestigatedindowntown MonteAltoCity,SãoPauloState,Brazil,inproximitytothecityhallbuilding,themainchurch,con- dominiumsandmarketingestablishments.Onehundredseventyfourpalmtreesof10specieswere investigated,inwhich72specimensofRhodniusneglectus,apotentialChagasdiseasevector,werecap- turedviamanualmethods.Allinsectswerecollectedfromdeadleaves,organicdebrisandbirdnests intheonlythreeLivistonaaustralispalmtreesinthecentralparksquare.ThiswasthefirstrecordofR. neglectuscolonizingthispalmspecies.AlthoughnoTrypanosomacruziwasfoundbyabdominalcompres- sionfollowedbylightmicroscopy,thepoornutritionalstatusofthebugshamperedtheexaminationof gutcontentsforparasitedetection.Furthermore,thecentralcrownsofthetrees,whichshelterbats(Chi- roptera:Mammalia),couldnotbecarefullysearchedforinsectsduetodifficultaccess.Thisnewfinding highlightsthesuddenalterationininsectbehavior,probablyasaresultofman’sinterference.Thisreport aimstowarnthoseinvolvedinthehealthsystemaboutthisnewthreat,justifyingdetailedresearchof theareatoevaluatethemagnitudeofthisemergingpublichealthissue.
© 2013 Elsevier B.V. All rights reserved.
Chagas disease afflicts millions of people throughout Latin America,yetnovaccinehasbeendeveloped.Thisdiseaseiscaused byaprotozoanparasite,Trypanosomacruzi,transmittedtoman mainlybyinfectedblood-suckingbugs,thetriatomines.Itisesti- matedthat betweenseventoeightmillionpeoplecarryChagas disease, placing this illness among the most serious parasitic diseaseinthesouthernhemisphere(WHO,2010).Theepidemi- ological scenariofor this diseaseis continuouslychanging, and recently,Abad-Franchetal.(2013)questionedthecertificationof theabsenceofChagasdiseasetransmissionbynativevectorsin Brazil.Infact,inCearáState,adomestictransmissioncyclewas disclosedas20%ofalldogsinoneperiurbanlocalitywereT.cruzi positive(Limaetal.,2012).
∗ Correspondingauthor.Tel.:+551633016943. E-mailaddress:[email protected](J.A.daRosa).
The establishment of endemic Chagas disease requires man/triatomine cohabitation in homes (Schofield and Galvão, 2009).Somespecies of Rhodniusadapt todomiciles (e.g.Rhod- niusprolixius),whereasthemajorityarestrictlysylvatic.Rhodnius neglectusmaybein betweentheseadaptationstatuses,because coloniesofthisspecieshavealreadybeenreportedindomiciles ofruralareas(Abad-Franchetal.,2009).However,theconsensus is thateven a sylvaticspecies representsa threat,asa popula- tionportionoftheseinsectswillnaturallyendupinvadinghomes or landing on food,usually attracted by artificial lights(Abad- Franchetal.,2009;Gurgel-Gonc¸alvesand Cuba,2007).Thereis onehypothesistoexplainthehighindexes(insomespotsover 10%)ofhumanT.cruziserologicalprevalenceintheAmazonbasin, aspeoplemaybecomeinfectedbybitingoraccidentally,through infected food(e.g.ac¸aíor sugarcane juice) contaminated byT. cruziinfectedtriatomines(Coura&Borges-Pereira,2012),which hasbeenresponsibleforoutbreaksinsomespotsotherthanthe Amazon(e.g.SantaCatarinaState;Steindeletal.,2008).
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populationofdwellingsinvadedatnightbyinsects,supposedCha- gasdiseasevectors.Thesenotificationscamefromtheurbancenter, morespecificallyfromthe14thfloorofabuildinglocatedinfront ofasmallwoodedpark(∼11,500m2)inthecentralsquareofthe
city.Therefore,ataskforceinvolving(i)thecityhealthsurveil- lanceservice,(ii)thecityhalland(iii)thelocalsuperintendenceof endemicdiseases(SUCEN)madeitpossibletocarryoutaninvesti- gationofthepalmsinthecentralsquare.
MonteAltocity(21◦ 10′ 34′′ S,48◦ 33′ W)islocated374km
fromthecapitalofthestateofSãoPauloandhas46,642inhabitants withinanareaof347km2(IBGE,2012).Theannualrainfallrateis
1441mm(Agritempo,2012)andtheannualaveragetemperature is21.5◦C(PrefeituraMunicipaldeMonteAlto,2012).Therehave
notbeenanytriatominereportsinhumandwellingssince2003 (Wanderleyetal.,2007).Therefore,sincethelocalpopulationas wellasvectorandmedicalsurveillancesystemsarenolongerused todealingwithChagasdiseaseanditsvectors,theinitialsearchwas performedsuperficially,characterizedbyanextremecaretoavoid anydamagetothepalmtrees(e.g.pullingoffortearingliveleaves). Therefore,thisinspectionwasrestrictedtodeadpalmleaves,bird nestsandvegetationresidue.Unfortunately,itwasimpossibleto carefullyinvestigatethecrownsofthepalmsduetodifficultaccess. Asaresult,174palmtreesof10specieswereinvestigated:Caryota urens,Coccothrinaxbarbadensis,Dypsislutescens,Dypsismadagas- cariensis,Livistonaaustralis,Livistonachinensis,Phoenixroebelenii, Syagrusromanzoffiana,RoystoneaoleraceaandRoystonearegia.The searchinglabortookthreeworkingdays(atotal of∼24h).Five men,sharedthetask:onemanclimbedamechanizedmobilelad- dertoremovedeadleaves,birdnestsandvegetationdebriswhile theotherssearchedforbugsineverythingthatfelltotheground.
Ofallthepalmstreespresentinthesquare,onlythethreeL. australis(Fig.1)werepositivefortriatomineswiththismethod- ology,providingthe72collectedbugs(25males,22females,13 fourthstageand12fifthstagenymphs),allofwhichwereidenti- fiedasR.neglectus,accordingtoLentandWygodzinsky(1979).It wasimpossibletodeterminehowmanybugscamefromeachtree becauseleavesandorganicdebrisgotmixedafterfallingdown. However,liveinsectsweresurelyseeninallofthesethreetrees duringtheinspection.Thedistancesbetweentheinfestedpalms andtheinvadedbuildingweremeasured,aswellasthosefromthe palmstotheclosestresidualforests,whichshallbeinvestigated regardingthepresenceoftriatomines(Figs.2and3).
Animportantfeature ofL. australisis that itsleavesremain attachedtothetrunkforalongtime,evenafterdyingand dry- ing,whichfavorsthemaintenanceofbirdnestsandorganicdebris. ThiswasthefirstrecordofR.neglectusassociatedwithL.australis palms.Hitherto,R.neglectushadbeenonlyfoundinpalmsofthe generaMauritiaspp.andAcrocomiaspp.(Abad-Franchetal.,2009; Dias,2000;Gurgel-Gonc¸alvesandCuba,2007;BatistaandGurgel- Gonc¸alves,2009).InCearáState,Limaetal.(2008)establishedfor thefirsttimeanunusualassociationbetweenR.nasutusandthe Licaniarigida(Oiticica)tree,a largeleafytreeoftheChrysobal- anaceaefamily.Valenca-Barbosaetal.,inpressreportedalsofor thefirsttimeTriatomabrasiliensiscolonizingcacti.R.nasutususu- allyinhabits palm trees, speciallyCopernicia prunifera, whereas T.brasiliensishadbeenconsideredexclusivefor rockyoutcrops.
Almeidaetal.(2009)claimedthatthisbehavioralterationsmight be a result of man’s environmental interference and has been increasinglyevidentformanytriatominespecies.Thismightbe asynanthropizationprocess,suchasT.sherlocki,aspeciesprevi- ouslyconsideredexclusivelysylvatic,howeverrecentlydetected colonizinghomesinaquarryminingcommunity.Thiseventmight bealsoappliedtothenoveloccurrenceofR.neglectusinL.australis inaveryurbanizedarea.
Fig.1. LivistonaaustralisspecimensfromwhichR.neglectusspecimenswerecol- lected.
Professionals from SUCEN, Ribeirão Preto (SP) staff, exam- ined the insects by abdominal compression, followed by light microscopyinordertoverifythenaturalinfectionbyT.cruzi,butall specimensprovednegativefortheprotozoan.However,mostofthe insectswerewithpoorgutcontents,whichcompromisesareliable parasitedetection.Furthermore,molecularmethodsarerequired toassurethenaturalinfection,becausesomeinsectsmaypresent alowparasiticburden(Ramseyetal.,2012).Inaddition,bugscol- lectedmighthavebeennegativebecausetheywereallencountered inproximitytobirdnests,birdsbeingrefractorytoT.cruziinfec- tion. However,bats (Chiroptera: Mammalia) inhabitthe crown ofthetrees(A.Vedoveli,municipaldepartmentofepidemiolog- icalsurveillance;personalcommunication,September10,2013), andopossums(Mammalia:Didelphimorphia),themostcommonT. cruzisynanthropicreservoir,arenaturallyabundantinurbanareas, especiallyparks.
Aninspectioninthecrownofthetreesisstillrequired,andwe suspectthatonlyaportionofthetriatominepopulationwascaught, asthosesupposedtobeinthecentralcrownofthetreesevaded thiscaptureeffort.Weconsiderthepossibilitythatthecrownsof otherpalmtreespeciesarealsoinfested.Toanswerthisquestion, live-baitadhesivetrapsadaptedfortriatominecapture(fordetails, see:Noireauetal.,1999;Abad-Franchetal.,2000)willbeapplied forallpalmtreesinthearea.Limaetal.(2008)collectedanaverage of3.9triatominesperinfestedpalmwiththiskindoftrapinCeará State.
SomeMonteAltoneighboringcities(e.g.Arac¸atubaeBirigui) havealreadypresentedrecordsofR.neglectusformingdomiciliary colonies.Ofspecialinterest,aR.neglectuscolonywasdiscovered onthe10thfloorofanapartmentbuildinginArac¸atuba,where20 firstandsecondstagenymphswerecaptured(theprecisedatewas
Fig.2.AerialpictureofMonteAltocitytakenbyGoogleEarth,accessedonOctober8,2012.Distancesfromtheinfestedpalms1and2(PL1andPL2)andthebuildinginvaded (B)bytriatomines:PL1–B:83.70m;PL2–B:50.94m.
Fig.3.AerialpictureofMonteAltocitytakenbyGoogleEarth,accessedonOctober8,2012.Distancesfrompalms(PL)andtheclosestresidualforests(F1,F2andF3):PL1– F1:429.00m;PL1–F2:464.00m;PL1–F3:1146.00m.ForPL1andPL2definition,gotoFigure2.
notavailable;Rodriguesetal.,2009).Giventhattheepidemiologi- calscenarioisnotstatic,thefactthatR.neglectusspecimenswere presentinanurbancenterfromMonteAltocityis,perse,area- sonforconcern(Costaetal.,2002;López-Cárdenasetal.,2005; Rodrigueroand Gorla,2004).Micro-foci ofChagas diseasehave beenattributedtoeitherresidentialtriatomineinvasionsorfood contamination,incriminatingseveralspeciesofnativetriatomines, which may result in sporadic transmissions or even outbreaks (Abad-Franchetal.,2013).
Asstressedabove,thelackofnaturalinfectionforthiscapture techniquedoesnotmeantherearenoinfectedbugsinthisarea. ThelastnationalserologicalsurveyforChagasdisease,performed from2001to2008(Ostermayeretal.,2011),declaredthatthere wasnoacuteChagasiccaseinchildrenunderfiveyearsold(V.M. Costa,BrazilianDepartmentofEpidemiologicalSurveillance;per- sonalcommunication,September09,2013)intheentireSãoPaulo State.Howeveranelementoftheepidemiologicalchannel(thevec- torinthis case)arrivesin anon-endemic place,anunprepared populationisvulnerableatseverallevels:(i)torecognizethevector, (ii)todiagnoseacutecasesofthedisease,(iii)toapplybasiccontrol measuresand(iv)topreventthedisseminationofthisnewhaz- ard.Afutureprojectwillinvolvevectorsearch/surveillance,health educationand collection aswell ashandlingof wildmammals
withtheparticipationofspecializedstaff(mammalogists,medical veterinariansanddoctors).Therefore,thisfindingwarrantsmulti- disciplinaryresearcheffortsinthisareatoevaluatethispotential emergingpublichealthissue.
FinancialSupport
CAPES (AUXPE – Parasitologia – 1528/2011, process num- ber23038.005285/2011-12)andFundac¸ãodeAmparoàPesquisa doEstadodeSãoPaulo,Brazil(processnumbers2010/50.355-1, 2010/17027-0and2011/22378-0–Fapesp).
Acknowledgments
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