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Rabies in humans and non-human in the state of Pará, Brazilian Amazon

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braz j infect dis.2013;17(2):251–253

The

Brazilian

Journal

of

INFECTIOUS

DISEASES

w w w. e l s e v ie r . c o m / l o c a t e / b j i d

Brief

communication

Rabies

in

humans

and

non-human

in

the

state

of

Pará,

Brazilian

Amazon

Marcus

Emanuel

Barroncas

Fernandes

a

,

Lanna

Jamile

Corrêa

da

Costa

a,∗

,

Fernanda

Atanaena

Gonc¸alves

de

Andrade

b

,

Lucila

Pereira

Silva

c

aInstitutodeEstudosCosteiros,UniversidadeFederaldoPará,Braganc¸a,PA,Brazil bInstitutoFederaldeEducac¸ão,CiênciaeTecnologia,Tucuruí,PA,Brazil

cLaboratóriodeRaiva,LaboratórioNacionalAgropecuárionoPará/LANAGRO,Belém,PA,Brazil

a

r

t

i

c

l

e

i

n

f

o

Articlehistory:

Received24August2012

Accepted7October2012

Availableonline9March2013

Keywords:

BrazilianAmazon

Humansandnon-humans

Lyssavirus

Rabies

a

b

s

t

r

a

c

t

Weevaluatetherelationshipofpositivecasesofrabieswiththecontinuingexpansionof

livestockproduction,andanalysethetrendsofthiszoonosisinhumanpopulationinthe

stateofPará,BrazilianAmazon.Thedistributionofrabiescaseswasrecordedbetween1999

and2004.Of148casesofrabies,21%wereinhumansand79%innon-humanmammals.

Therapidgrowthinlivestocknumbersseemstobeassociatedwiththeincreaseofpositive

casesinbovinelivestocktransmittedbyvampirebats.Thisideaissupportedbypositiveand

significantrelationshipofbotheventsintime(p<0.01),butfailedwhenspatialdistribution

amongregionsofthestatewasconsidered.However,rabiescasestendtooccurtowardthe

northeasternofthestateofPará,whererabiescasesareproportionallyfivetimesgreater

thanothermesoregions,suggestingthatincreasedlivestockproductionmayinfluencethe

increaseofthiszoonosis.

©2013 ElsevierEditoraLtda.Allrightsreserved.

Rabies,causedbyLyssavirus,isadiseasefoundinhumansand

severalothermammalspecies.1,2Upuntilthemid-1990s,the

stateofPará,easternportionoftheAmazon,hadthe third

highestrateofrabiescasesinBrazil.AccordingtotheBrazilian

HealthMinistryonlyninecasesofrabiesinhumans

(trans-mittedbyvampirebats)wererecordedinParábetween1999

and2002,allinthesoutheasternportionofthestate.By

con-trast,from2003to2004,thenumberofrecordedcasesmore

thandoubledto22,andwasmorewidespread,rangingfrom

thesoutheasttothenortheast.Therefore,thepresentstudy

wasconductedprimarilytoassesswhetherpositivehuman

andnon-human(cattle)casesofrabieswereassociatedwith

Correspondingauthorat:InstitutodeEstudosCosteiros,UniversidadeFederaldoPará,CampusdeBraganc¸a,AlamedaLeandroRibeiro

s/n,Aldeia,Braganc¸a,PA68600-000,Brazil.

E-mailaddress:lannacorrea@yahoo.com(L.J.C.daCosta).

theongoingexpansionofthebovinelivestockproductionin

the region,andtoevaluatecurrenttrendsinhumanrabies

incidenceinthispartoftheBrazilianAmazon.

All positivehumansamples (n=31) resultedfrom

infec-tionsthatoccurredinruralareas.Thenon-humangroupwas

represented bycattle (n=117). Rabieswas diagnosed using

directimmunofluorescenceassaysandviralisolationthrough

theintracranialinoculationofthecentralnervoussystemof

newbornmice.Positivesampleswereidentifiedusing

mono-clonalantibodies.

The distribution of the rabies cases (human and

non-human) was recorded in the different mesoregions of

1413-8670/$–seefrontmatter©2013 ElsevierEditoraLtda.Allrightsreserved.

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252

braz j infect dis.2013;17(2):251–253 Mesoregions 1 = Lower amazon 2 = Marajó 3 = Belém 4 = Northeast 5 = Southwest 6 = Southeast Key Human Non human 1999 - 2000 0 50100200300 400 Km 6 5 1 2 4 3 1 2 4 3 2001 - 2002 2003 - 2004 5 6 1 N 2 4 3 5 6 N N 57º0’0’’W 3º0’0’’N 0º0’0’’S 3º0’0’’S 6º0’0’’S 9º0’0’’S 54º0’0’’W 51º0’0’’W 48º0’0’’W 57º0’0’’W 54º0’0’’W 51º0’0’’W 48º0’0’’W 57º0’0’’W 54º0’0’’W 51º0’0’’W 48º0’0’’W 0 50100200300400 Km 0 50100200300 400 Km 3º0’0’’N 0º0’0’’S 3º0’0’’S 6º0’0’’S 9º0’0’’S

Fig.1–Positivehumanandnon-humancasesinintervalsoftwoyears,from1999to2004,inthesixmesoregionsofthe stateofPará,easternBrazilianAmazon.

Pará between 1999 and 2004 (Fig. 1). Annual variation

and differentgeographic regions were bothevaluated with

respect to the number of rabies cases in human and

non-humanbyusingKruskal–Wallis’snon-parametric

anal-ysis of variance (H), while linear regression (with data

transformed) was applied to describe the relationship

betweentherabiescases(humanandnon-human)and

live-stockproduction,consideringannualandmesoregion

varia-tions.

Between1999and2004,148casesofrabieswererecorded

in Pará, of which, 31 (21%) were in humans, the

remain-ing117(79%)innon-humanmammals(cattle).Thenumber

ofnon-humancasesvariedsignificantlyamongthesix

geo-graphic regions of the state (H=9.94; df=5; p<0.01), with

themajorityofcasesbeingrecordedinthesoutheast(n=62;

42%). On the other hand, no significant differences were

foundintheannualvariationfornon-humancases(H=2.12;

df=5; p>0.05), although mostcaseshave been reported in

2003and2004.Regardinghumancasestherewasno

signif-icant differences forboth annual variationand geographic

regions (H=9.8; df=5; p=0.07 and H=3.05; df=5; p=0.69,

respectively), with half of cases recorded in the Marajó

mesoregion.

TheproductionofbovinelivestockintheBrazilian

Ama-zonbasinhasincreasedprogressivelysince1991.According

totheParáStateDepartmentofAgriculture(SAGRI),thelocal

bovine herdincreased annuallybyan average of12%

dur-ingthepresent studyperiod(1999–2004)totaling 73,181,447

individuals,reaching thepeak in 2004(24%). Similarly,the

numbersofrabiescasesincattlehavenoticeably grownin

thesameyear(n=62).Thus,itseemsreasonabletoassume

thatthisrapidgrowthinlivestocknumbers,mainlyin2004,

maybeassociatedwiththeincrease inthe figures of

posi-tivecasesofrabiesinbovinelivestocktransmittedbyvampire

bats, Desmodus rotundus. In fact, the regression analysis

between these two events showed a positive and

signifi-cantrelationship intime(regression, F=25.8;df=5;p<0.01

– Fig. 2) supporting this hypothesis, but failed when

spa-tialdistributionamongregionsofthestatewasconsidered

(regression, F=5.63;df=5;p=0.07).However,it isimportant

toemphasizethatthesoutheastmesoregionhasalivestock

ten timeshigherthan theNortheast,wherethenumberof

rabiescasesisproportionallyfivetimesgreaterthanthatof

southeast.

Asaconsequenceoftheincreaseofpositivecasesincattle,

onewouldexpectahighernumberofrabiescasesinhumans

inruralareas.However,regressionanalysisrevealed

signifi-cantcorrelationsofhumancasesneitherwiththeincreaseof

rabiescasesincattle(regression, F=0.44;df=5;p=0.54)nor

40 35 30 25

Positive bovine livestock

20 15 10 5 8 10 12 14 16 Bovine livestock (x106) 18 y=3.461x - 22.71 R2=0,86 F=25.88; p<0.01

Fig.2–Relationshipbetweenpositiverabiescaseson bovinelivestockandtotalbovinelivestockfrom1999to 2004inthestateofPará,BrazilianAmazon.

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brazj infect dis.2013;17(2):251–253

253

withtheincreaseoftotalbovinelivestock(regression,F=4.44;

df=5;p=0.10).

RabiesoutbreaksinthestateofParáhaveoccurredinrural

areas,wherethemajorityofthehumanpopulationlivesin

relativepoverty.Mostvictimsreportedin2004,forexample,

livedinthatchedhouses,withnoelectricityorotherutilities,

andnotcloseofwaterbodies.Inmostcases,informationwas

availableonlyfortheconfirmedcasesbygovernmental

enti-tiesandnotforallclinicalcases,i.e.,thefiguresofpositive

individualswereunderestimated,whichisabarriertomore

accuratelydefinethe trendsofthis disease intheAmazon

region.

Oncehumans dwellinthefocusareaofbat-transmitted

rabies,structuralchangestriggeredbynon-biologicalorsocial

factors makethedisease emerge.3 In fact, therabies virus

maybespreadingrapidlyoverwideareaswithintheAmazon

basinandbeyond,especiallythroughintraspecies

transmis-sionamongbatpopulations,4despitethelowoccurrenceof

thistypeoftransmission.5

The association between vampire and other bats, and

wild batrabies iswell documented atmany South

Ameri-cansites,4,6 but thelackoffield surveysand monitoringof

batpopulationshinderthe understandingofthespreading

processand transmissionrouteswithintheAmazonbasin.

Additionally,theactivitiesofsurveillanceanddiseasecontrol

alsodependoninformationaboutthesizeofforestedareas,

topography,hydrographyandlandusebyman,5,7beingsuch

factorsstraightlyrelatedtothelivestockindustry.

Conflict

of

interest

Allauthorsdeclaretohavenoconflictofinterest.

Acknowledgements

WethankthelaboratorypersonneloftheSecretariaExecutiva

de Saúde Públicado Pará (SESPA) – Núcleode

Epidemiolo-gia (NUEP), Instituto Evandro Chagas (IEC)– Departamento

de Raiva,and the Agênciade DefesaAgropecuáriado Pará

(ADEPARÁ)inthestateofPará,Brazil,whohaveacquiredand

contributed thesedataover manyyears.Weare gratefulto

MauraE.M.Sousaforherassistancewiththefigures.

r

e

f

e

r

e

n

c

e

s

1. BarbosaTS,MedeirosDBA,daRosaEST,etal.Molecular

epidemiologyofrabiesvirusisolatedfromdifferentsources

duringabat-transmittedhumanoutbreakoccurringin

AugustoCorreamunicipality.BrazAmazonVirol.

2008;370:228–36.

2.HuR,TangQ,TangJ,FooksAR.RabiesinChina:anupdate.

VectorBorneZoonotDis.2009;9:1–11.

3.SchneiderMC,RomijnPC,UiedaW,etal.Rabiestransmittedby

vampirebatstohumans:Anemergingzoonoticdiseasein

LatinAmerica?RevPanamSaludPublica.2009;25:260–9.

4.Salmón-MulanovichG,VásquezA,AlbújarC,etal.Human

rabiesandrabiesinvampireandnon-vampirebatspecies,

SoutheasternPeru,2007.EmergInfectDis.2009;15:1308–10.

5.MayenF.HaematophagousbatsinBrazil,theirroleinrabies

transmission,impactonpublichealth,livestockindustryand

alternativestoanindiscriminatereductionofbatpopulation.J

VetMedBInfectDisVetPublicHealth.2003;50:469–72.

6.MattosCA,FaviM,YungV,etal.Batrabiesinurbancentersin

Chile.JWildlDis.2000;36:231–40.

7. GomesMN,MonteiroAMV,LewisN,etal.Landscaperisk

factorsforattacksofvampirebatsoncattleinSãoPaulo,

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