h tt p : / / w w w . b j m i c r o b i o l . c o m . b r /
Veterinary
Microbiology
Isolation
of
Salmonella
spp.
in
cattle
egrets
(Bubulcus
ibis)
from
Fernando
de
Noronha
Archipelago,
Brazil
Marcio
A.
Silva
a,b,c,∗,
Érika
F.S.T.
Fernandes
a,
Sandra
C.
Santana
d,
Maria
Fernanda
V.
Marvulo
c,e,f,
Mércia
R.
Barros
a,
Sineide
M.O.
Vilela
a,
Eliane
M.F.
Reis
g,
Rinaldo
A.
Mota
a,
Jean
C.R.
Silva
a,caUniversidadeFederalRuraldePernambuco,DepartamentodeMedicinaVeterinária,Recife,PE,Brazil bParqueEstadualDoisIrmãos,Recife,PE,Brazil
cInstitutoBrasileiroparaMedicinadaConservac¸ão,Recife,PE,Brazil
dAdministrac¸ãodoDistritoEstadualdeFernandodeNoronha,Recife,PE,Brazil eFaculdadeMaxPlanck,Indaiatuba,SP,Brazil
fUniversidadePaulista,Campinas,SP,Brazil
gInstitutoOswaldoCruz,FIOCRUZ-RJ,LaboratóriodeEnterobactérias,RiodeJaneiro,RJ,Brazil
a
r
t
i
c
l
e
i
n
f
o
Articlehistory:Received4July2017
Accepted14January2018
Availableonline3March2018
AssociateEditor:CristianoGallina
Moreira Keywords: Ardeidae Oceanicislands Conservationmedicine Enterobacteriaceae Publichealth
a
b
s
t
r
a
c
t
Thegrowthofthepopulationofcattleegrets(Bubulcusibis)inthearchipelagoofFernando
deNoronhaconstitutesathreattopublichealthandbiologicaldiversitybecauseoftheir
competitionwithandpredationonnativespeciesandthepossibilityoftransmissionof
pathogenstohumanbeings,livestockandnativewildlife.Theaimherewastosearchfor,
isolateandidentifyserovarsofSalmonellainclinicallyhealthylocalcattleegrets.Cloacal
swabswereobtainedfrom456clinicallyhealthycattleegretsofbothsexesandavarietyof
ages.Theswabsweredividedinto51pools.Sixofthese(11.7%)presentedfourserovarsof
Salmonellaentericasubspeciesenterica:SalmonellaserovarTyphimurium;Salmonellaserovar
Newport;SalmonellaserovarDuisburg;andSalmonellaserovarZega.Onesamplewas
identi-fiedasS.entericasubspeciesentericaO16:y:-.Resultsinthisstudysuggestthatcattleegrets
maybereservoirsofthisagentonFernandodeNoronhaandrepresentarisktopublichealth
andbiologicaldiversity.
©2018PublishedbyElsevierEditoraLtda.onbehalfofSociedadeBrasileirade
Microbiologia.ThisisanopenaccessarticleundertheCCBY-NC-NDlicense(http://
creativecommons.org/licenses/by-nc-nd/4.0/).
∗ Correspondingauthor.
E-mail:[email protected](M.A.Silva).
https://doi.org/10.1016/j.bjm.2018.01.004
1517-8382/©2018PublishedbyElsevierEditoraLtda.onbehalfofSociedadeBrasileiradeMicrobiologia.Thisisanopenaccessarticle
Introduction
Exoticinvasivespeciesareanimalsand/orplantsthathave
beenintroducedintoaplacewheretheydidnotpreviously
exist naturally. They are one of the biggest threatsto the
environment, causing enormous harm to biodiversity and
tonaturalecosystems.Furthermore,theymaypresentrisks
tohumanhealth,giventhattheymaytransmitdiseases to
endemicspeciesandcauseecologicalimbalances.1,2
FernandodeNoronha isanarchipelagocomposed by21
oceanicislandswith26km2oftotalareathatarepartofthe
BrazilianstateofPernambuco.Theyarelocatedinthe
equa-torialzoneoftheSouthAtlantic(3◦5028.9S,32◦2439.4W),
atadistanceof545kmnortheastwardsfromRecife,thestate
capitalofPernambuco.Themainislandhasaresident
pop-ulationofapproximately2930inhabitantsandisdesignated
asaMarineNationalParkandanEnvironmentalProtection
Area.3,4
Amongtheexoticinvasivespeciesseeninthearchipelago
of Fernando de Noronha, cattle egrets (Bubulcus ibis) have
causedemerging problems.2 Theseincludecompetition for
resources and predation of endemic species; potential for
transmissionofdiseasestothehumanpopulationand
pro-ductionanimals;andpotentialforcollisionswithaircraft.2,5,6
CattleegretsbelongtothefamilyArdeidae,order
Pelecan-iformes.Theyareinsectivorousandarecommonlyobserved
foraginginopenfield areas,closetocattle,andfeedingoff
insectsthatdisturbthecattle.7Thefirstreportsofoccurrences
ofthisspeciesonFernandodeNoronhadatefromthe1980s,
andtherehasbeenexponentialgrowthofthepopulationsince
then.2
Amongthepathogenstransmittedbywildbirds,Salmonella
spp.hastakenonanimportantroleandhasevenbeen
indi-catedasathreattowildlifeconservationingeneralterms.8,9
Salmonellabelongs to the family Enterobacteriaceae; it
col-onizes the intestines of reptiles, birds and mammals and
hasgreatimportanceinrelationtobothhumanandanimal
pathology.9,10 Some serovars like Typhimurium and
New-port arecommonlyassociatedtofood poisoningorenteric
infectionoutbreaksworldwide,beingagreatthreattopublic
health.8–10,24,28,30,32,34
Presence of this genus has been reported in several
bird species and groups, such as domestic poultry,11,12
Psittaciformes,13,14 ratites,15,16 raptors,1 Passeriformes18,19
and Ardeidae.8,10,19–23 Incattle egrets,Salmonellahas
previ-ouslybeenisolatedonlyintheUnitedStates.8,19,23,24
Considering the scarcity of studies on isolation of this
enterobacteriaincattleegrets,theaimherewastosearchfor,
isolateandidentifyserovarsofSalmonellainclinicallyhealthy
birdsinthearchipelagoofFernandodeNoronha,Pernambuco,
Brazil.
Material
and
methods
Studyarea
Thecoveredareaofthecompostingunitofwastetreatment
stationinthemainislandofthearchipelagoofFernandode
Noronhawasusedasthesiteforcatchingcattleegrets.
Capture,physicalrestraint,clinicalexaminationand collectionofbiologicalmaterial
BetweenDecember2007andJuly2008,456cattleegrets(B.ibis)
ofbothsexesandvariousageswerecaught.Thebirdswere
attractedintothecoveredareaofthecompostingplantbythe
presenceofprey(larvaeand insects).They werecontained
there by closing the doors and were physically restrained
byusingnetsandglovessuitablefortheprocedure. Allthe
birds weresubjected toclinicalexaminationatthetimeof
capture.25Aftertheyhadbeenconfirmedasclinicallyhealthy,
sterileswabs(CBProducts,Corumbataí,SãoPaulo,Brasil)were
introducedintothecloacaofeachbird.Thoseswabswere
sub-sequentlykeptunderrefrigerationandsenttothemainland
inStyrofoamboxescontainingrecyclableice,nomorethan
48hafterwards,forlaboratoryprocedurestobeperformed.
Laboratoryprocedures
Thelaboratoryanalysesrelatingtoisolationand
identifica-tion were performed inthe Infectious-Contagious Diseases
Laboratory of the Department of Veterinary Medicine of
theUniversidadeFederalRuraldePernambuco(UFRPE).The
swabs weredivided into pools ofnotmorethan 10 swabs,
inaccordancewiththeorderofcaptureofthecattleegrets,
thus totaling 51 pools. To isolate the agent, the classical
scheme for investigating Salmonella recommended by the
NationalProgramforPoultry-rearingHealth(PNSA)wasused.
This involved use of 1% buffered peptone water (Oxoid®,
Cambridge, England) as a pre-enrichment medium and
tetrathionate (Oxoid®,Cambridge,England)and
Rappaport-Vassiliadis(Acumedia®,Lansing,Miami,USA)asenrichment
broths, with subsequent seeding into brilliant green
(Bio-brás Diagnósticos®, Montes Claros, Minas Gerais, Brasil)
and xylose lysine deoxycholate (XLD) (Oxoid®, Cambridge,
England)selectiveagars.Coloniesthatwerecharacteristicfor
SalmonellawerecrushedintothescreeningmediumTSI(triple
sugarironagar)(Oxoid®,Cambridge,England),whichenabled
presumptiveidentificationofthegenus.26,27
Simplified biochemical profiling was used, consistingof
characterizationoftheisolatesaccordingtotheircapacityfor
decarboxylationoflysine,useofcitrateasthesolesourceof
carbon,mobilityandproductionofhydrogensulfide(H2S)and
indoleinthefollowingmedia:lysineironagar(LIA)(Biobrás
Diagnósticos®,MontesClaros,MinasGerais,Brasil),Simmons’
citrateagar(Oxoid®,Cambridge,England),ureabroth,methyl
redbroth(Oxoid®,Cambridge,England),VogesProskauer(VP)
(BiobrásDiagnósticos®,MontesClaros,MinasGerais,Brasil)
andsulfideindolemotility(SIM)agar(BiobrásDiagnósticos®,
MontesClaros,MinasGerais,Brasil).28
Afterbiochemicalprofilehadbeenconfirmed,thesamples
weresenttotheNationalReferenceLaboratoryfor
Enterobac-terialInfections(LRNEB)ofInstitutoOswaldoCruz,FIOCRUZ,
RiodeJaneiro.Atthislocation,antigencharacterizationwas
performedbasedonserologicalclassificationof
Kauffmann-WhiteandLeMinor,withrepresentationinaccordancewith
thecriteriaofGrimontandWeill.29Alltheantiserausedinthe
Table1–Salmonellaserovarsisolatesfrom51poolsofcloacalswabsfromcattleegrets(Bubulcusibis)ofarchipelagoof
FernandodeNoronha,Pernambuco,Brazil,2008.
Identificationofpool Numberofcattleegrets Serovar
P10 10 SalmonellaentericasubspeciesentericaO16:y:–NDa
P13 10 SalmonellaentericasubspeciesentericaO16:y:–NDa
P20 10 SalmonellaserovarDuisburg
P42 4 SalmonellaserovarZega
P45 9 SalmonellaserovarNewport
P47 6 SalmonellaserovarTyphimurium
a ND,undetectable(flagellatestructureundetectableafterphaseinduction).
Noneofthecattleegretspresentedanyclinicalsignsofsalmonellosis,suchasruffledfeathers,fever,edemaordiarrhea.Allthebirdspresented weightswithinthenormalpatternforthisspecies,rangingfrom272to543g.
Results
Outofthe51poolsanalyzed,27 (52.9%)presentedcolonies
suggestive of Salmonella spp. Among these 27 pools, after
confirmation through biochemical tests, six (11.7% of the
total number of pools) presented test results compatible
with the genus Salmonella, and all of these were
subse-quentlyconfirmedthroughserotyping(Table1).Presenceof
fivedifferentserovarswasconfirmed:Salmonellaserovar
Duis-burg; Salmonella serovar Zega; Salmonella serovar Newport;
Salmonellaserovar Typhimurium;and onesample thatwas
identifiedasSalmonellaentericasubspeciesentericaO16:y:-.
Discussion
Theabsenceofclinicalsignsofsalmonellosisandthegood
bodyscoresofthecattleegretsthatwerecaughtdemonstrated
thatallofthemwereclinicallyhealthy.Someofthebirdshad
previouslybeenringedaspartofecologicalstudiesconducted
previouslybyprofessionalsattheBrazilianNationalCenterfor
ResearchandConservationofWildBirds(CEMAVE).However,
nopreviousstudiesoninfectiousorparasiticdiseasesinthese
birdsonFernandodeNoronhawerefound.
Most of the studies that have described isolation of
Salmonella in cattle egrets were conducted in the United
States.Intwostudies,thegenuswasidentifiedbut notthe
speciesorserovar.21,23 SerovarsofSalmonellaincattleegrets
were described inthreestudies.8,19,24 Locke atal.8 isolated
SalmonellaserovarTyphimuriumfromtheinternalorgansof
asingle individual cattle egret that had been heldin
cap-tivityanddied ataresearchcenterinMaryland.Thesame
serovarwasalsoisolatedfromotherbirdsinthefamily
Ardei-daethatdiedduringthesameoutbreakofsalmonellosis:little
blueheron(Egrettacaerulea),greategret (Ardeaalba),snowy
egret(Egrettathula),tricoloredheron(Egrettatricolor)and
black-crownednightheron(Nycticoraxnycticorax).Allofthesespecies
alsoformpartofBrazilianfauna.5
Phalenetal.24isolated30differentserovarsofSalmonella
injuvenileandadultcattleegretsthatwereculledfor
popula-tioncontrolpurposesatvariouscollectionpointsinTexas,and
observedthecharacteristics ofthesebirds’ bacteremiaand
death.Callawayetal.19isolatedSalmonellaserovarMontevideo
fromthe cecumofcattleegrets,underisolationconditions
greatlyresemblingthoseofthepresentstudy.Serovars9
iso-latedfromcattleegretsofFernandodeNoronhaseemednotto
causeillnessesinthesebirds,whichcorroboratedthefindings
ofCallawayetal.,19whosestudyincludedclinicallyhealthy
birds.
AmongtheSalmonellaserovarsfoundincattleegretsof
Fer-nando deNoronha,the serovarTyphimurium wastheonly
one similar to those found byPhalen et al.24 inthe same
speciesin TX,UnitedStates.Thus, thepresent report
pro-videsthefirstdescriptionofoccurrencesofserovarsDuisburg,
ZegaandNewportandofonesamplecharacterizedasS.
enter-icasubspeciesentericaO16:y:-,incattleegretsinBrazil,and
particularlyonoceanicislands.
S.enterica subspeciesentericaisfrequently isolatedfrom
poultry, exotic birds, pigs and chicken carcasses, and has
becomeespeciallycommonsincethelatterpartofthe20th
century. TheserovarEnteritidisistheonemostcommonly
encountered.12,30 On the other hand, S.enterica subspecies
entericaserovarO16:y:–hasnotbeen isolatedinother
stud-ies,evenfrompoultry,althoughsomeauthorshavereported
isolationofS.entericasubspeciesentericainassociationwith
otherserovarsinpoultryandlivestock.11,24
Bada-Alambedjiet al.31 isolatedSalmonellaserovar
Duis-burgfromtwoofthe75samplesthatwere positiveforthis
genus,fromchickencarcassesthatwerebeingsoldin
mar-ketsandopenfairsinDakar,Senegal,andotherserovarswere
isolatedfromtheremainingsamples.HoszowskyandWasyl30
isolatedSalmonellaspp.fromseveralpoultryspeciessuchas
chickens,turkeys,ducks,geese,pheasantsandpigeonsand
from exotic birds. However, in comparisonwith the
num-bers of isolations ofother serovars, it was foundthat the
Duisburg serovar had lowfrequency ofoccurrence.Like in
the presentstudy,theabovementionedtwostudiesdidnot
showanyindicationsofillnesscausedbythisserovarinthese
birds.
The prevalenceof Salmonellaserovar Zega inwild birds
seemstobelow,giventhescarcityofstudiesdescribingthis
agent.Evenincasesinvolvinghumans,theprevalenceseems
to below.32 Onthe other hand, the serovarsNewport and
Typhimuriumseemtobemorecommonandtohavegreater
potentialtocauseillnessinanimalsandhumans.8,10,24,28,32
From the point of view of animal health, cattle egrets
habituallycomeinto closeproximitytocattle,sheep,goats
andhorses,6,7whichsuggeststhattheymayserveassources
of infection for humans and livestock.5,6 Several authors
have suggested that contact between synanthropic birds
forSalmonellato poultryspeciesand consequently totheir
carcasses.24,31,33
Thus,cattleegrets mayperform thisrole ofasourceof
SalmonellainfectiononFernandodeNoronha,withdispersion
ofserovarsisolatedinthisstudytothehumanpopulationand
todomesticandwildanimals,bymeansoffecal
contamina-tionoffoodsourcesornaturalandartificialwaterreservoirs
suchasmillponds,watertanksandcisterns,wherethesebirds
habituallylandtocatchinsectsandsmallamphibians.This
possibility has already been described by other authors in
otherlocalities.5,10,17,25,33,34
Regardingpublichealth,Salmonellaspp.hasbeenshown
to be the main agent of foodborne diseases in Brazil
and worldwide17,24,35 and any of its serovars may be
involvedinoutbreaksoffoodpoisoninginfectionswithmild
symptoms.9,12,17,28,30 The serovarsdescribed inthe present
study have little importance as causative agents for
non-typhoid enteritis in humans, with the exception of the
serovars Typhimurium and Newport, which are commonly
associatedwiththistypeofillness.8–10,24,28,30,32,34
Inrelationtobiodiversityconservation,pathogenic
sam-plesofSalmonellaspp.may presentrisksofhigh morbidity
andmortalityamongwildanimals,9withconsequentlossof
geneticvariabilitywithinpopulations.Thismaygiveriseto
evenmorecriticalproblemsforendangeredspecies,thereby
acceleratingtheextinctionprocess.20HallandSaito10 cited
Ciconiiformesastheorderofbirdsrankedasthirdmost
sus-ceptible todeathdue to salmonellosis.However, regarding
salmonellosisorinfectionbySalmonellaspp.inwildbirds,the
majorityofauthorshavestatedthatthesebirdsaremore
com-monlyasymptomaticcarriers.20,22,25Itshouldbenotedthatin
2014,thefamilyArdeidaewasrelocatedfromtheorder
Ciconi-iformestotheorderPelecaniformes.25
Although the most native marine birds of Fernando
de Noronha are not endangered species, infected cattle
egretsmayhaveanegativeimpactthroughtransmissionof
Salmonellatothesespecies.Throughcompetitionfor
ecologi-calnicheswithnativespecies,presenceofcattleegretsmay
thusincreasethemortalityratesamongthelocalavifauna2,5,6
iftheSalmonellaserovarsthattheycarryhappentocause
dis-easeoutbreaksinthelocalpopulationsofwildbirds.
Even though there have not been any reports of
out-breaks of salmonellosis in the avifauna of Fernando de
Noronha,itwould beprudentnottodismissthis
hypothe-sis, giventhat there isno in-depthknowledge ofthe wild
epidemiological chain of this disease in this locality, and
considering the pathogenic potential of isolates found in
thiswork.8–10,24,28,30,32,34Thus,itispossiblethatcattleegrets
reallyareactingasreservoirsand/ordisseminatorsofthese
pathogensontheseislands.Thedataobtainedinthisstudy
areofrelevanceforpublichealth,sincetheycontributetoward
environmental monitoring through knowledge of the
epi-demiologyofSalmonellaserovarsencountered.
Conflicts
of
interest
Theauthorsdeclarenoconflictsofinterest.
Acknowledgements
The research was supportedby the Administrationof
Fer-nando de Noronha, state district, Pernambuco state. The
authorsarealsogratefultotheInstitutoChicoMendespara
Conservac¸ão da Biodiversidade (ICMBio), and to the
Labo-ratóriodeEnterobactériasofFIOCRUZ-RJ,forserotypingthe
samples.R.A.Mota,andJ.C.R.Silvareceivedfellowshipsfrom
theNationalResearchCouncil(CNPq),Brazil.
r
e
f
e
r
e
n
c
e
s
1.PadillaLR,Santiago-AlarconD,MerkelJ,MillerRE,ParkerPG.
SurveyforHaemoproteusspp.,Trichomonasgallinae,
Chlamydophillapsittaci,andSalmonellaspp.inGalapagos
Islandscolumbiformes.JZooWildlMed.2004;35:60–64.
2.NunesMFC,Barbosa-FilhoRC,RoosAL,MestreLAM.The
cattleegret(Bubulcusibis)onFernandodeNoronha
Archipelago:historyandpopulationtrends.RevBrasOrnitol.
2010;18:315–327.
3.IBAMA–InstitutoBrasileirodoMeioAmbienteedos
RecursosNaturaisRenováveis.Brasília,DF:Planodemanejo
doParqueMarinhodeFernandodeNoronha;1990.
4.InstitutoBrasileirodeGeografiaeEstatística–IBGE.
EstimativadaPopulac¸ão.2016Accessed09.03.2016.
5.SilvaMA,MarvuloMFV,MotaRA,SilvaJCR.Aimportânciada
ordemCiconiiformesnacadeiaepidemiológicadeSalmonella
spp.paraasaúdepúblicaeaconservac¸ãodadiversidade
biológica.PesqVetBras.2010;30:573–580.
6.LunardiVO,Oliveira-SilvaCC,LunardiDG.Synanthropic
characteristicsofthecattleegretBubulcusibis(Linnaeus,
1758)intheBraziliansemiarid.BrazJBiol.2013;73:669–670.
7.DellaBellaS,Azevedo-JúniorSM.Considerac¸õessobrea
ocorrênciadagarc¸a-vaqueira,Bubulcusibis(Linnaeus)(Aves,
Ardeidae),emPernambuco,Brasil.RevBrasZool.
2004;21:57–63.
8.LockeLN,OhlendorfHM,ShillingerRB,JareedT.
Salmonelosisinacaptiveheroncolony.JWildlDis.
1974;10:143–145.
9.CarvalhoVM.Colibaciloseesalmonelose.In:CubasZS,Silva
JCR,Catão-DiasJL,eds.Tratadodeanimaisselvagens:medicina
veterinária.SãoPaulo:Roca;2014:1389–1398.
10.HallAJ,SaitoEK.Avianwildlifemortalityeventsdueto
salmonellosisintheUnitedStates,1985–2004.JWildlDis.
2008;44:585–593.
11.HoferE,SilvaFilhoSJ,ReisEMF.Prevalênciadesorovaresde
SalmonellaisoladosdeavesnoBrasil.PesqVetBras.
1997;17:55–62.
12.TessariENC,CardosoALSP,KanashiroAMI,StoppaGFZ,
LucianoRL,CastroAGM.OcorrênciadeSalmonellaspp.em
carcac¸asdefrangosindustrialmenteprocessadas,
procedentesdeexplorac¸õesindustriaisdoEstadodeSão
Paulo,Brasil.CiêncRural.2008;38:10–16.
13.KanashiroAMI,CastroAGM,CardosoALSP,TessariENC,
TavechioAT.PersistênciadeSalmonellaspapós
antibioticoterapiaempsitacídeospertencentesaum
criadourocomercial.ArqInstBiol.2002;69:99–101.
14.RojasMJ,RejoMGT,MasdeuV,AcostaI.Hallazgos
bacteriológicosymicológicosenavespsitácidas.RevCubana
CiêncAvíc.2002;26:125–128.
15.MarinhoM,MeirelesMV,SouzaAVG.Determinac¸ãoda
microfloradotratogastrintestinaldeavestruzes(Struthio
camellus)criadosnaregiãonoroestedeSãoPaulo,
16.PereiraRA,CanalCW,SchmidtV.Detecc¸ãodeSalmonella
Anatumemema(Rheaamericana).CiêncRural.
2008;38:823–825.
17.MillánJ,AdurizG,MorenoB,JusteRA,BarralM.Salmonella
isolatesfromwildbirdsandmammalsintheBasque
Country(Spain).RevSciTechOffIntEpiz.2004;23:905–911.
18.PennycottTW,ParkA,MatherHA.Isolationofdifferent
serovarsofSalmonellaentericafromwildbirdsinGreatBritain
between1995and2003.VetRec.2006;158:817–820.
19.CallawayTR,EdringtonTS,NisbetDJ.Isolationof
EscherichiacoliO157:H7andSalmonellafrommigratory
brown-headedcowbirds(Molothrusater),commongrackles
(Quiscalusquiscula)andcattleregrets(Bubulcusibis).Foodborne
PathogDis.2014;11:791–794.
20.SavidgeJA,SileoL,SiegfriedLM.Wasdiseaseinvolvedinthe
decimationofGuam’savifauna?JWildlDis.1992;28:206–214.
21.GrantKR,WatsonJ.Controllingnuisanceegretandheron
rookeriesinOklahoma.In:TwelfthGreatPlainsWildlife
DamageControlWorkshopProceedings.1995.
22.León-QuintoT,DeLaVegaA,LozanoA,PastorS.Summer
mortalityofwaterbirdsinamediterraneanwetland.
Waterbrids.2004;27:46–53.
23.PhalenDN,DrewML,ContrerasC,RosetK,MoraM.Naturally
occurringsecondarynutritionalhyperparathyroidismin
cattleegrets(Bubulcusibis)fromcentralTexas.JWildlDis.
2005;41:401–415.
24.PhalenDN,DrewML,SimpsonB,RosetK,DuboseK,MoraM.
Salmonellaentericasubsp.entericaincattleegret(Bubulcusibis)
chicksfromcentralTexas:prevalence,serotypes,
pathogenicity,andepizooticpotential.JWildlDis.
2010;46:379–389.
25.FontenelleJH,BarrosLA.Ciconiiformes,Pelecaniformes
GruiformeseCariamiformes(Maguari,Tuiuiú,Garc¸a,Socó,
Guará,Colhereiro,Jacamim,Saracura,Frango-d’água,Groue
Seriema).In:CubasZS,SilvaJCR,Catão-DiasJL,eds.Tratado
deanimaisselvagens:medicinaveterinária.SãoPaulo:Roca; 2014:441–455.
26.MinistériodaAgricultura,PecuáriaeAbastecimentodo
Brasil–MAPA.Brasília,DF:ProgramaNacionaldeSanidade
Avícola;2002.
27.PaivaJB,SterzoEV,RiberioSA,PereiraEA,BerchieriJuniorA.
IsolamentodeSalmonella:comparac¸ãodasetapasde
pré-enriquecimentoeenriquecimentodiretodeamostrasde
fezesarmazenadaspor24e96horas.ArqInstBiol.
2006;73:263–269.
28.FortunaJL,FrancoRB.Pequenodossiêepidemiológicoda
Salmonella,comocausadoradeinfecc¸õesalimentares.Hig Alim.2005;128:33–43.
29.GrimontPAD,WeillFX.AntigenicformulaeoftheSalmonella
serovars.Paris,France:WHOCollaboratingCentrefor
referenceandresearchonSalmonella;2007.Accessed
09.03.16.
30.HoszoswskyA,WasylD.Salmonellaserovarsfoundin
animalsandfeedingstuffsin2001andtheirantimicrobial
resistance.BullVetInstPulawy.2002;46:165–178.
31.Bada-AlambedjiR,FofanaA,SeydiM,AcampouAJ.
AntimicrobialresistanceofSalmonellaisolatedfrompoultry
carcassesinDakar(Senegal).BrazJMicrobiol.2006;37:
510–515.
32.HealthProtectionAgency.Salmonellaserotypesrecordedinthe
HPASalmonelladataset:JulytoSeptember2003.London,UK:
C.D.R.Weekly;2003.
33.Andrés-BarrancoS,VicoJP,GarridoV,etal.Roleofwildbirds
androdentsintheepidemiologyofsubclinicalsalmonellosis
infinishingpigs.FoodbornePathogDis.2014;11:
689–697.
34.KangM-S,JeongO-M,KimH-R,JangII,LeeH-S,KwonY-K.
Athritisinanegret(Egrettaintermedia)causedbySalmonella
Typhimuriumanditspotentialrisktopoultryhealth.JWildl
Dis.2015;51:534–537.
35.NadvornyA,FigueiredoDMS,SchmidtV.Ocorrênciade
Salmonellasp.emsurtosdedoenc¸astransmitidaspor
alimentosnoRioGrandedoSulem2000.ActaSciVet.