Transcript of Babesia gibsoni Infections in Dogs - CORE
Babesia gibsoni Infections in Dogs
Yamane Itsuro, Conrad Patricia A., Gardner Ian journal or
publication title
The journal of protozoology research
volume 3 number 4 page range 111-125 year 1993-10 URL
http://id.nii.ac.jp/1588/00001679/
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Keywordsβabesia gfbsonlaninedogs′anemiababesiosis
At‡STRACT
lNTRODUCnON
Babesia glbsoTZha5aWidegeographicdistributionTbblelrmemajority
OEreported⊂aSeShavehistori⊂allycomefromAsia′howevehedistributionof
Bgibsonlseemstobein⊂reaSlngOduyeandDipeou1976Andersonetal1979
Boussarie1982Conrad et al1991Because oflimited restrietions on the
importationoEhealthydogsthatareasymPtOmaticearrierOfBgfbsonE′this
parasiteappearsEohavebeenintroducedintonewcountries′SuChastheUnited
StatesCrovesand Yhp1968Andersonetal1979Conradetal1991
Previousreviews oftheliterature relevant toBgEbsoniarelimitedand′
Withtheex⊂ePtionofoncJapancsereviewNoda1977havefailedtoconsider
βAβEJA CJβSOJINCTIONSINXXS
myofepepubhdinOEngli1angua8ejou nepfe WWerendtrormphehe′jl tlntita
emphaskon diibdhod1didiIme′ tdc1
UISll11UUltr1
CIJMLSIGNS Nahalictiom
idimakl5F119he19f y∝ykmdlxmmKmdal19SumetaL19
Q1Cr19pdnVdqmdOk19 Abud1Itohamdlbhlw¢veddurimgtk⊂Ourddini1
dedpgDie⊂tddtIle OfdiaSecIyindiedbymiamybe autable to1e
Yilthparieisoh2tkbts aubre5istandorctrd
i′ad3dOftentwhababaddddg
1
‾
βAβEJA G50JINFECTONSIN DOGS
Tablc 1
WorldwideDistributionotNaturaesfdgInrcction5a
H8 Rferenc CDun
1 0 1 1 1 I
1 ′ 1 1 J l J 1 1 1 ′ 1 1 l J l l J 1 J 1 ′ 1 1 l l l
Palto
Ledier
lzeki Inanib Kihara Kiharaetal SumaetaI Nodaeti Okuda OkuyamaOkuda
FWt11elal Yonamineeal Jabnetal 1Dh elaI
SneViraa nevirana et aL Seneviratna
Levine
l
Japan
l † 1 1 1 1 1 1 1 1 1 1
1953
19‘1
WaS¢8PluredinTimtute11hSudanwhihwa5fenamd
Emes5
Hepatomaly
¢ U 8 4 2 1 k U 4 n V b 4 4
1 1 1 1 1
0 n V 3 h ′ Q n V 5 2 J 4
l l † l
repqrtedt
hdudedarestudiesthaSPeCifica11ymentjonlleabsenceoftheclinical
SIghSindicated e Pyrexibdylemrature39115
bloodengorgementinSPlenicredpulpHildebrandL19811n⊂reaSedplasmacel15
extramedullary hematopoleSis andor hemosiderosisWere Observedin the
5pleOf8gf5ifedgSeneYiatnal95∂Hildebrd1191
Hemosiderosis′a5Wellasicterus and hemoglobinuriaare the TeSult
ofthe
exeSSiveerythrocyticdestructionwhid10eCurSinbabesiosisLiverdysfunctioh
rcsultingindecreasedbilirubinmetabolismmayalsoacceleratetlledevelopment
OfieterusinBgibsonEine⊂teddogsSdlalmetal1975Althoughthepresen⊂e of
Eree hemoglobin may glVe urine a brownish eoIorthese slnS arelisted
SeParatelyinTable2beauSemanyinvestigators eitherrLOted
thepresenceof hemoglobinuriaInaniba1956SiJlha arLd Chosh19861toh et
al1987or observed brownCOlored ulineKihara et al1964Farwe11et
al1982Itohnd
Itoh1990withoutcommenting onthepresence oftheotherfeaLureIn one
StudytJrinalysISuSlngahemogobindetectionstriprevealed that70flldog
with mild clinialslgnS and yelowish brown to browm01oredllrine had
hemo81obinuriaItohetal1987TheabsenceEhemoglobinuriawasspeeifically
BABESIA GLBSONINFECTIONS7N DXS
notdbysomeinvesLigatorsPatton1910Seneviratna1953Kiharaetl1964
CroveandYap19′however′thefrequeneYandmethodsoEtestingusedto
makethisdeterTnirtationwerenotreportedNo1977hOtdinhisreviewthaL
heTnOglobinuriawascommoninpureeddDgSinfectedwithBgtbso”iohen
theitlfedoWiucedintpW areaS Whemany anima15Were
susceptibletoinfeetiom bYeOntraSt′0rscontendedthathem10bitluriaand
icerWeun0ImOninβinfedSnat196G Dennk1972
Wieepn8anmia′kmatologkt⊂anbemnrd
typlCalofgβectkms∂rendweudometdthdevdand
Tedp⊂dlocbhavebeObdhacukinreomkeM19
raetal19Smaetal19Ok19Cde1991′btheisn nSistdkpattemvere tkomboba was
a00mmO ding′ObsVdin90flOnaItyindqComd1991mdha7
experimentallyinfbeteddogsConradjurtPublisheddata1925reported
lhaLbloodcbtaihedfrominfbetedddgshadprolongedcoagulationtime′Whieh
mayhavebecnduetothromboeytopeniahalIotherrepoindudedi
eViewJthrombocYteCOuntSOrCOaguLationhctorsofnaturallyihEecteddogswere
taSSe5dowcommonlymbobpia∝ugiiie⊂
inothereountriesandhowtheparasiteeausesthisteTationrequiresfurther
evaluationi
DogswithatuEeBgibsoniinfectionsmaybemisdiagnosed ashaving
autoimmune hemolytic anemia becauOE the similaritYin1inical5igns
FarwelLetal1982roundLhat25of28dogsnatura11yinfededwithgibsonjhad
pQSitiveresLstotheantiglobulinCoombstestWhidltheyaEtTibutedtothe
prodution of antibodies against altered surEae antigens orL ParaSid
erythroyteS Afterrecovery′200fthesedogswereretesledand1365had
naer′deitetkktenαOfparasiShthblodTkre′
differentialdia8nO5isothesediseasesmaybemoreofaprobleminacuterather
an dlrOnicinctim
Xpimenalin ildbyintedHcbmderexr
Some of the usLefulinformation thatan be obtained by evaluaLtiort
of exmti∝ddWhiwemOrddugeOWSedfdisea5e
ineludelhetimefrominfediontotheappeararLCeOEparasitesprepatentperiod′
correhtionbetweenparasitemiaandpyrexiaandtheeffeetoFsplenectomyonthe
out00meOfeinfe⊂tn¶mmittediedoOfgfbdpk 0or12⊥dadrs
Swamhathand5hoHt193
and711days wih Otsuka1974 There was eonsiderable variationin the
prepatent periods observed whcn dogs wer
i1aledwithinfederyhrotesdependjngupon theroule8rinfeIion′ number of
paratesintheinQltlm and whether the⊂e11s were fSh or
ryOPfServedFeXample′ 55dogsinoculaedIV wifrhgf
eryhr∝yhadprephtpedsramgfrom229daysmean85day5and48
dd8SgivenaSCi1umhadprepatetpe∫iodsof940daymean15dayS Ray
andIdnatni1943Prepatent periodswere similarin spleenintact arLd
middotWereg1VenaSimilarhDCt11mofinederythrocytes
bytIlameroulVorIPGrovesId Demis72Botrosetal1975Anderson
eal199
PyreXia was oberVed before parasiles re deteed 50m
perlmenallyinddognevira19aHara197In8urXpmemtal
StudiesIiOIving5splenetOmi2X2dand2spleenintaetdoPyrQXia390Cwas
notobservedtlntila1loEthedogshddetectablepaTaSitemialnEhisandoLher
Sdie5′lhere was naPPantmIiorlbetwee¶PyreXia and theleve18f
ParaSiemiaRayandldnani1943Serteviratna1965aGroveand Dennis1972
etal19 Manyd5iftedbyimoculationof8gpfed
ylesfeporledlyfailedtodevelopmarkedpyrexiaPan1910Nodaetal
19To1989ortheyhadonlyinermitentfeverSeneviratna1965aHara1971
Botrosetql1975InsevereinEectiqnsthebodytemperatureofinEeteddog
maydeαeetO360CpriortodeatbPatton1910Hara1971kahashietal 19
Theimporta⊂eOfthespleincontTOllinggi8nfetioni5made
appareTltby⊂OmParingtheseveritYfdiseaseinspIenectomi2edamdspleenintat
dog5In comparative sudiesSPIee⊂tOmizedanidsn11develope4
paraSimiasof2190whereasspleentacaninalsn20hadparasmiasof
1204ohereal19To19Splemectomied dogSalso hadgher
Eataliratcs′Of76n34otrosetal1975toIOOn12Tbmuraetal1979
Tb1989COmParedwithllntreatedspleenintaetdogsinthesamestudieswhidl
hadratalirateSOf19n27
pIAGNOSTICMTHODS Definitive diagnosis of Babesia inlectians is most
often based on the
identificationoLparasitesonthinbl00dmearSStainedwithaRomanowskyin
Pat10rL191ORao1926Mahortey1977Fowlereta1970reportedthatFieJd’
tainhadadvanlaSOVerCimsa£taiIorthedetectinOgi5∂fkcau5ethe
ainlngtimewasshorerand tlltraStWaSbettq however′StaiIedsIides
fdedmbrequiekly hour experien⊂eCiemsaStainlng PrOVides for good
ViualizationoEBgtbsontinthinbloodsmearsWhereasrapidQuiekstairare
inadequar accurae parasileidentifi⊂ationProperstainlOrperipheral
bld5meaTSi5Criticalln tbe diagmsisofgsfinfetions′partict11ary
beeausetheparasitesaTtSmallandthepossibilitythatseverearLemiaandEaality
CanCCurWhenlessa2ofeeryrocyte5COntainparasitesAndersonetal 19
Anularforrns135mirOn5h1udiIlgrlng5andovals′are themost mmQn
mOrPhoIogie forms ofgibsoTiinperipheralbloodMaronpotand
Guilldy197Roller etal19 Othermorphoog‡⊂foTmSirdudeeloated long
formCOmmadotsanaplasmoidbodiesbandrod′ameboidpaired
pyriforms and quadrupletmalteserOSS′tetrad orpetaloidformsThe
proportionofeachmorphologiforrrtmayvaryaecordingtothestageofthe
infectionForexamplerNamikawaetal1988observedthatringformswere more
common attheinitialstageoftheinfectionandother formsSu⊂h as
eotmaameboid′PairedpyriEorrnandmaltaseformsappearedseveraldayslate
1zeki1925alsoreportedthatelongatedorbarEormsWhichrangedfroml245
micronsinlength′Wererareandusua11yappearedonlyattheteTmina15tageOf
infeetionIzeki1925AlthoughTnOStinfeetederythr∝yteSeOntainonlylor2Zl
gparaSitestheproportionofyhrocyteswithmullipleparasilesm
iSeSthepercentinfectedcellsparasilemiai5e5ltohandltoh19
resuling1naSmnyaS5Roheret1985or1630Palton1910parasiteswiin
anerythr∝yte
ThedetectionoEantibodiesto8gibso71iinthebloodofinfeeteddogscant
usedfordiagnosisParticularlylnChronicallyinfecteddogsthatmayhavelowoT
nodetetabIeparasitemiasTheindire⊂tEluorescerLtantibodyIFAtestluSirLg
infeetederythrocytesasantigen′isthemostextensivelyutilizedserodiagnostic
teslforgfbsfAndersonetal1980welletal1982Ohetal1987Conrad
etaI1991Yarnaneetal1993bNaturaIlyinfeeteddogsinlapanshowedtiters
rangingfroTrt40toIOJ240usingtheIFAtestFarwelletal1982ItohetaL1987
ThelowesttitertoBgfbsoT7Edetectedinanaturallyinfecteddogwithelini⊂al
babesiosisinCaliforniawasl′280and70f12dogshadtitersoflO240T20480
Yamaneetal1993bInotherexperimentalinfeetionsIFAtilersofl28012800
weredeteLedwithin25r35daysofinoeulatingZL
gtbsot7iinfeEederYthrocytes
Tbrnuraetal198OOgitanietal1983Kawamuraetal1987Morishigeeal
198
Anenzyme1inkedimmunosorbentassay testEuSAdevelopedfor
gjbsonihasalsoshownpromiseasaserodiagnostictesfJdetectingantibodiesin
thesera ofall18infeeted dogs testedandidentifying68uninfected
dogsas
negativeTo1989Nonetheles5thepotentialusefulnessoEthistestmaYbe
reduedbythefindingthatserafromBCanfsirLfeteddogsalsoreactedpo5ilivelY
toBgtbsoniantigensTb1989Antigeni”rOSSrea⊂itybetweenthetwocanine
BabesiaspedeshasalsobeenreportedwiththeIFAndersonetaL1980Yhmane
etal1993bandindireethemagglutinationtestsRisticetal1971andshouldbe
takenintoconsideraLionwheninterpretingtheTeSultsoEtheseseroIogicte5tSIn
ourstudies′OnedogthatwasexperimentallyirLfeetedwjhZ3developedarL
IFAtiterof16010BgibsonftIoweveTldogsthatwereexperirnenta11yinfected
withBgEbso”idevelopedrOreaCtivetitersof320to640tocqnLsandtiters
rangingfroml′2801010′240to T gdif andgβr C
Yamaneetal1993bTheseTeSulLsindieatethaIsomedogswithgfbsoTL
infectionsm8ydevelopfalsepositivereactionsir1FAteststothesccIoselyrelated
CaninepaTaitesmeyalsosuggestha15erOdiagnosisoesepara5ite5maybe
improved by theidentification and
utilizationofparasriteSPe⊂iianLigen5in tlterdefinedELISSIs
TbappropriatelylnterPretBgfbsonEIFAandl∃LISAtestresultsfurther
inEormaLionis needed about thepersistenceofantibody titersin
ehrorLically infe⊂tedanimalsThepersisEen⊂eOftiLersindogs
thathaverecoveredfrom
gEbsoTZiinfectionshasnotbeenwe11documentedTwoexperimentallyinLected
dogsinourstudiesdevelopedpeaktitersof4D960and81920toBgibso”iwithin
thefirst120dayspostTirFcctionandtheirtiterspersistedat1O240for268to284
daysmaneetal1993bSimil1y′theikrsof3aturallyinfecleddoa Were
mOitoredrera618mons period persisted at10′240Thomford′
unpubli5heddata
meapplicatioOfmole⊂ularbiolbglCaltechniquesWhichdonpIrqulTe
thedetedionofantdiesmayalsoprovetobeusefubrpisof ginfecio
ganbegenolyplCallydi5timishedm
dermOrPhoIoglaIlysimilarbabeialparasite5uSlnatjNprobethtWa
Pmduedbypmerhainf8CtionPCneamplificationofal6Sike
rRN′genqueneNAiromrffDNConradetal1998asedoIl
thisuα′aPCRdtionstemWaSdevplopedandsu∝e5Ilymployed
reidemtificationof∴kbloodofinfe⊂ledhumaSpSietal
1992AtpTeSentWeafeWOrkingtoidenlifygfirDNAsuenC
ahddevelopaSimiIaTPCRba′5eddenStemfortpa5iteinaead
Cbronia1yinfe⊂teddqgs
TREATMtNT
ThemostpromiirlgdruforthetreatmentofBglbsonLinLe∈tionsarethe
diamidine derivativesPeeifieallydiminaene aCeturale′ phenamidine
isethionateandpentamidirLeisgthionateHoweveTlauthetherapetlticdnlgtrials
nalurallyinfecteddogsdidnothaveeonlroldSWlhwereinftedWi
5adwereuntfealedTherefore′alevaluationofdrefa⊂y
rertSisdirultbecau5einEecteddogsmighthaLVereOVeredwithouttretmtnt
Further1ihi1trialswhichiIICludelfeadaldnontreaddogareIleededb
prQγideoeedataondrugeffia⊂
1969Okuda1969OkuyamaandOkuda1970S00tLetal1971Farwelletal1982
hal1987Conradetall1andexperimentalicionBauer19
wleret∂119Rue1973kahashietal1984in1een1nactdSIIl the
experimentalinfectionsmOStOL the treaEed dogs survived whallth
etrOldSdiedn5foreadlgTOFowlereal1972Rurfet193ora
lowefatalitywrepOrledimtt05ancrOl2grollpSkabashe al198
Howevediminaeneratelreatmetdid noIprevendeatin
AABESIA GIBSONI INFECTIONS IN WGS
experimentallyinfected splenectomized dogsILoh et al1988Conrad′
unpublisheddataFornaturallyinfecteddogsPentamidineisethionateat165
mgkgtwicein4hours was aseipus a5treatmeWith diminaene
aeturaehowever′itsefficacymaybeques′tionablesin⊂einfeeddogswith8ut
treatmentcontrolgroupwerenotincludedinthisstudyFarwe11etal1982
Fhenamidineisethionate admimitered at165mgkg twicein24hoursalso
pTOVedemaiousagainstmentallyinfecteddhowever′therelVaSOnly one
controldogiJl1udedin this study and this dogalsoIrVived without
treatmentPCrove5and Vanniasingham1970Ruffetal1973reportedhal
experimentallyinfe⊂ted dogs which re⊂eivedintramus⊂uLarlnJeetiorLS
OE phenamidineisethionale10mgkgand5mgkg′3daysapartordiminazene
aceturateon⊂eatllmgkghadreducedfatarity1owerparasitemiasandhigher
packedcellvolumesaftertreamentthndiduntreateddogsortho5etreatedwith
niridaOlequininesulfateordapsonen5foreachgTOuPAlthoughrecovery
generallybegan5hortlyaftertheinitiationoftreatmenwithal130fthese
diamidine derivativesParaSites5fi11persisEed atlowlevels andor
relapse
parasitemiaso⊂urredwitln2mDnthstolyearposLLreaLmentGrovesand
Vanniasingham1970Scottetal1971Farwelletal1982Ttohetal1987Conrad
etal91
Niridazole′metrOnidazole and parvaquorte haveshown some efTieay
agaitgβ owleretal19showedredu⊂edfatalityratesidogs
treatedwithniridazoIesingleoraldoseof5OOmgormetronidazole250mg
daily forlO daYSJalthough the bestclinicalresponses were obLained
with
diminalCneaCeturateIna1Other⊂OmParativedrugtrial′niridazolewasfoundto
haveminimalaetivityainstBgLbso”fRuffetal19731Thkahashietal1984
reportedthatdogsexperlmePtallyinLectedwith8gibOniWhichweretreated
withparvaquone20mgkg′OnCeSChadabeLterclinicalresponsethandiddogs
lhat were treated with diminazene aceturate1O mgkgSCtWicein24h
imidocarbdiproprionate2O mgkgSCtWicein24hor aOmbinationof
5ulphadiazine25mgkgandtrimethoprim5mgkggivenorallyfor7day5and
nofttreatmenLOntrOldogsn5EoreachgroupParVaquOnehasprovenefficaey
againstTgfrgrf PγandTOfcat1eMoanandMcHaTdyl2
Unsurnetal1988The⊂losephylneticrelationshipofBAgEbsqnttothese
eilerlalspeciesThomford′PerSOnalcOmmunicationmaY eXPlain why
ParVaquOneiseffeetiveagalnSt Blgonibutisminimallyeffe⊂tiveagalnSt
melaTgeβbgsspedes
1n additiort to chemotherapyreOVerY from canine babesiosis may be
failitaled bY the administration of supportive treatmenEs
sudla5blood
transfusionstorepla⊂elo5terythrocytesandnuidtherapytocorrectdehydration
aidosis and azotemiaNoda1977Breitschwerdt1984Itoh et al1987
AdminstratiorL
PREVENTIONANDCONTROL
Tn addition to tick transmissionBgibsoniinfeetionsmaybeacquired
transplacentallyAbuetal1973orbyb100dtransmissionlzeki1925Botrosetal
1975Andersortetal197merefofe′theinfe⊂tionstatu50fpregnantbitchesand
blooddonordogsshouldbeassessedbYeXaminationofstainedbcodsmearsamd
OlCaltestingforantibodiesto
Edueationofdogowner5andveterimriansabouttherisksandmethodsof
COntrOinggi8iinfectionsisvitaltoee⊂ive⊂OntrOlpr∈ramSBecauseof the
easy transportation of doS from endemic to nonendemic areas and
abundaneOftikinmanyplacesintheworinfectionsanbeeasilys‡readon
aglobals⊂aeSurveysofdiseaseprevalenetikdistributions′andanalysISOn
riskf∂CtOrSaSSOdated withinfectionareimportanlepidemiologl⊂aldataw
CanPOtentiallyprovideadditipnalstrategitOCOntrOlthespreadofinfEions
Quarantineandserologictestingofimporteddog5maybejustifiedtoprevent
irLfeetionspreadingtocountriesappareTltlyfreeofintection
ACKNOWLEDGEMENTS
BABESA CZ3SONJNFECTlONSIN DOGS
REIEIIENCS
bu′M′Hara′1NaitoShibauchi01973BabesinetionsinpuppleS
probablyduetotransplaentaltransmis5ionuiChikusanShEnpouVet
Md609ZO320iN
Anderson1F′MagnarelliLDonmerC′Spi2an′APiesman′J1979
CanineBabesLanewtoNorthAmerj⊂aScience20414311432NE
AndersonF′Magnarelli′LASulzerAJ1980L CaninebabesiosisIndirect
fluoresentantibodytestforaNorthAmericanisolateofBabesiagibsoniAm7
f4l2102215E
Atilola′MA0DipeoluOO1983StudiesonthedegreeofparasikmiaarLdthe
morphologlCalformsofBabesiaduringcrisesinspleneetomizeddogsZbL
Med303232iN
BauerFL1967ZurChemotherapiederBabcsLagibsonEInfeetionbeiHundenZbL
VdMdL1417018
BotrosbAMMochRWBarsoum′IS1975SoTneObservationson
experimenlallyindtlCedinectionodogswithBobesELgLsonip AmVetlRes
369396E
BoussarieD1982UncasdepiropLasmoseavedesparasitesdunaspe⊂t
particulierLIAnimaldeCompagnie17597599N
reiEschwerdtE1984BabesiosisPP7968O5I”Clinicalmicrobiologyand
infectiou5diseasesCreeneCEd′WDSaundersCompany′Philadelphia
ConradPAThornford1WYamane′IWhitingJDosmaLUnoTHoIshuh
HJShelly′S199lrIemolytiaemia⊂auSedbyβginfectionin
dSAydkdAβC19960l605N
Conrad′PA′Thomford1WMarshATelfordlTTSRAnderson1FSpielman
A′Sabin7AYamanePersing′DtI1992RibosomalDNAprobefor
differentiationofBabesfaTnfcrotiand BgibsoniisolatesCliT7crobiot3O
12101215
DaltaSCA1941AnnualreportoEtheimperialveterinaryresearehimstitute′
Mukteswar′fortheypar193738f11571E
Farwell′CELeGrandEKCobbCC1982CliniealobservatiorLSOnBabesLa
g5fandinfectionsindogsJ1VdkdA8r180507 51lN
FowlerLRuff′MDHornoWJ190Modificationoffield‘sstainfor
examinationofgrowhformsofβgsg0A†JtγelRgs31107910
FowleTJLRufMDFernauRCFurushoY19728abesiagfbsoTZi
ChemotherapyindogsAmVeLRes3311091114
Groves′MCYapLF1968BabesfagLbsoT7EinadogJAmVctMedAssoc
153689694N
Grove5′MGVanniasinghamJA1970TreatmentofBpbesagibsouiinfe⊂tions
withplenamidineisethionateVgf86810E
CrovesMGDennis′GL1972BabesiagibsFieldandlaboratorystudiesof
Canineinfetion5ErJ31153159
Hara, I. 1971. Experimental studies on canine babesiosis. Bull.
Fac. Agric. gCiU22329392E
BABESIA GBSONIINFECTIONSIN DOGS
Hi18ebnPK1981meOanadvIarpaholyOfsiosisp′p4594
bSiSistic′MrJPEdAcademicPress′NewYork
Inaniba′S19AaSerertfcanineproplasmosis 2149859N
ltHihiSOgasawa′T′qraAKawamraS19SA
OutbakoI⊂anineba5i05jsinomoripre′fectlJdA40 1611N
1toh′HiguhiSKaWamura19neerfe10fdimiqaeaCetueon
SplenectomiddogswithfCP1794E
ItohN11dhS1989MorphQlogialob5erValioOfβd5gii
eryfhrocytesofnaturallyinfecteddog5JVgfMdA∝425N
Itoh′Nltoh′S1990caseoFeanibabesioi5posblydevelopedby
tramsplatalinfectionPyMeA4327ZN
keki′H1925CamineplTOplamisdbseedinOiaprefecrelβyr2 12N′E
JakonRRLipmb′TLohofSLaleTtfQr infeetnsJA∝162
KaptlrHR1943∴ChemotherapyofcanineplrOPlasmosisduetoBbesiag
JVgrJ1919905
KawamuraM′Maede′YNamioka′S1987MitogenicreOrLSibuitiesof
lympll∝ylesinanimebabesiQSbandtheefecb8fsplenectomyonitf
35110E
EiraS1963ApplionofdiminaeneaCetWatetOCaTlinepiroplasmo
CSppgd3141l141N
iIla′S0suka′HtumoH19AsdyoncanineplrOPlamaqinical
SymptOmSOraCanBppudJVMgde1714l142N
Le′MdierE1922Piropla8medurenardD’arriqueFg5 GraySigfgdeJig95N
LeYineN1971Taxo10myPfhepir1asmsTrSAMiSS90Z33
LeviileNDd1973Prot2OanFaraites8fDomesticAnimalsandoEMan
pp3334BuTgeSSPllblisirC8mpanyMinneapoli5′MinlleSOta
LeYi′NEd1985VetednaryProto001ypp118IowaStUniveTSity
PrAmes′10Wa
Money′DF197780besfaoEDomesticAnimalsPP152LtnParasiticProtoz
Kier′JPEd′AcademicPreNewYQrk
MtRRGuindy′E10PrearysudyoPattoin
wildrnivqresanddomateddS′inyptAmlR3179N
MQ′DWTMcHardy′N1982Cpmparisonofeantithdlerialectof
Wellcome993Carldhalofil10meVScf328
MorishigeTTakahahiK′AbeSlKurosawaT50nOda′M19Dete⊂tiomf
drulimmunecPlexiIldpgsinfetedwithgg0C Dryg12352
NamikawaKSunaga′FKannY198M8rphologyoe5gfin
CanineerythTOCyteSVd5f509368E
NiakArLWarMKhatibi′S1973CaninebabesiosisinrrarLTTOPAnimHLth
Prα5280204N
NodaRNoda′StIorie′MOnishiTShimakoshiMAkashiM1973
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Noda′R19CainebabesiosisJVgfdA∝30247251
Oduye00Dipcolu0019768loodparasitesofdogsirlbadan
ACl17311337N
OgitaniT′Okabe′TtIwamotolSasakjJN1983TheOurSeOfparasitemiaand
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βαJgrfoJ3873E
OkudaYl1969CanineplrOPlasmosisfoundinKitasetsuMountains′Osaka
prefe⊂tureC5SVefMgdJ50612241226N
OkuyamaTOkudaM1970CanineplrOPlsmosisinOsakaanditsErealment
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OtsukaH1974StudiesorLtranSmissionofBLZbesagbsoniPatton1910by
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jackal5PE∫3274280N′E
Persing′DHMathiesen′DMarshall′WFTelford′SRSpielmanThomEord
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Purne11′R1981BabesiosisinvarioushossPPZ563BabesiosissticM
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RajamanickanCWiesenhutterEZin′FHamidJ1985Theincideneeof
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Rao′MAN1926P5mdg0alon′1910dRes14785800E
RayHNId1ani′JLA1943ObservationsontheformsofBabesiaglbsoTZt
PauonirLthedogWithanoteonthesystematilPOSitionoftheparasiteJT7dL
VL13267273E
RiBrti⊂MLykinsDSmithAR1971Habestacafrlsand
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385392
RoherDPAnderson′JFNiel5en′SW1985Experimentalbabesiosisincoyote5
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RuffMDFowlerJLFernau′RCMatsuda′K1973Aetionof⊂ertain
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64145E
Sehalm′OW′Jain′NCCarroll′lLJ1975VeterinaryHemaLology3rded′Lea
Febiger′Philadelphia
∴‘I
E7JIE5J CIβSONLJNTECTlONSIN DOCS
St′MWler′ILff′MD1lsgffinfetionofadiIl JAydA551591121123N
Sem′SKThevedprofninepirasmifJ Scf 3353
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indpWithspiOtrypan’hoedJ38S474N
P15aSl11diPaltoh1910etionsinthedog
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SeVratnaP1985bStudiesofkβidg∂nreCOfdogsinCekn CJ131N
Shetty′KS1934Trtmentof’tPig58i′’wis1faenqlJVg 1141N
SintLPGhoshP1986Treatmentofeliniealcasesof⊂aninebabio5istndI
yd69497N
Suma1′bhihara′S′Sugase′a£iMTEnbashi′SIto′S′Iwamoto′ki
F1966SeriesOf1ikesymptom′buldinRokkoMouTltainsirlKol
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due18PP′5gfPaftamQhoundsoftheMadrash11nt′
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SymoTH1928d←verduetpPfrsβgfPattoninakemeIof
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TakahasK′umaW′T′noda′MNakaTFujita′J19Atiomol
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Tamura′TTakaha5hiKSonodaMKoiwa′MNaga5akiK979ffectQf
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Tamura′TTakathashi′K′SonodaMKoiwa′M1980TheindirectfluorCent
arLtibodytestasamethodfordetecthg LJCiryf8249
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UnsurenlH′urtdedeJACoksuK1988ETfe⊂tiven50Lparvaquoneinattle
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Yame′Gardne1ARyan′CP′LevyMUrri0JConradPAl3a
r85rVeyOfandrJfc“po11nddogs inC1iSubmitted10PrgVgf
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Yamane1Thomford′JWGardner′A′DubeyTPLevyMConradPA
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YamaneICardner7TelfordInSEIwardTHair′JAConradPA1993c
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Yonamine′HIthikiHHamakawaM′ShimabukurDTSugiyamaMlIsoda
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518N
Edesnatesstudiesonexperimentalinfection
Ndesignalesstudiesonnaalinfection
∴’1