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
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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
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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
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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 ClinicalsymPtOmSeSPeClallyliverfuhetionsOfexperlmentallyinfeeteddogs withJVgfdA5SOC265759E
Noda′R19CainebabesiosisJVgfdA∝30247251 Oduye00Dipcolu0019768loodparasitesofdogsirlbadan
ACl17311337N
OgitaniT′Okabe′TtIwamotolSasakjJN1983TheOurSeOfparasitemiaand developrnentofspedficantibodiesinthcdogsinoeulaEedwithsLagibsont βαJgrfoJ3873E
OkudaYl1969CanineplrOPlasmosisfoundinKitasetsuMountains′Osaka prefe⊂tureC5SVefMgdJ50612241226N
OkuyamaTOkudaM1970CanineplrOPlsmosisinOsakaanditsErealment fCs5ppVdMedJ515312313N
OtsukaH1974StudiesorLtranSmissionofBLZbesagbsoniPatton1910by ydgf5Neumann1901βFαCAgrfcM 2135937E
PattonWS1910PreliminaryreportonanewplrOPlasmfoundinthebloodofthe houndsoftheMadrashuntandsubsequentlydiscoveredinthebloodofthe jackal5PE∫3274280N′E
Persing′DHMathiesen′DMarshall′WFTelford′SRSpielmanThomEord JWConradPA1992Dete⊂tionomIibypolymerasechain reactiqnJClMicrβoJ302097103
Purne11′R1981BabesiosisinvarioushossPPZ563BabesiosissticM KreierJPEds′AeademicPres5′NewYork
RajamanickanCWiesenhutterEZin′FHamidJ1985Theincideneeof caninehaemato2OainPeninsularMalaysiaVetPmsitot17151157N
Rao′MAN1926P5mdg0alon′1910dRes14785800E RayHNId1ani′JLA1943ObservationsontheformsofBabesiaglbsoTZt
PauonirLthedogWithanoteonthesystematilPOSitionoftheparasiteJT7dL VL13267273E
RiBrti⊂MLykinsDSmithAR1971Habestacafrlsand Solubleandeorpus⊂ularantigensisolatedfrombl∞dofdogsZTParpsitol30 385392
RoherDPAnderson′JFNiel5en′SW1985Experimentalbabesiosisincoyote5 andcoydogsAmVgfR26E
RuffMDFowlerJLFernau′RCMatsuda′K1973Aetionof⊂ertain antjprotozoalcompoundsagainstBLZbesiagibsonindogsAmVetResT34 64145E
Sehalm′OW′Jain′NCCarroll′lLJ1975VeterinaryHemaLology3rded′Lea Febiger′Philadelphia
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SintLPGhoshP1986Treatmentofeliniealcasesof⊂aninebabio5istndI yd69497N
Suma1′bhihara′S′Sugase′a£iMTEnbashi′SIto′S′Iwamoto′ki F1966SeriesOf1ikesymptom′buldinRokkoMouTltainsirlKol VMedAβ193653N
Swaillah′CSShoHE193TharlhrOdvedororsfβgdJ Jde525499503E
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SymoTH1928d←verduetpPfrsβgfPattoninakemeIof f8XburldsinIndiaJVe42682N
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Tamura′TTakathashi′K′SonodaMKoiwa′M1980TheindirectfluorCent arLtibodytestasamethodfordetecthg LJCiryf8249
To′M1989tlasicsttldiesonthescreeningtestforthedeveloprnenOEnewdrugs againsaninebabesiosisNipponVnimiUnivThe
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Yamane1Thomford′JWGardner′A′DubeyTPLevyMConradPA 1993bEvaluationoftheindirectfluorescentantibodytestfordiagnosisof nsindogs AJ15791584E
YamaneICardner7TelfordInSEIwardTHair′JAConradPA1993c Ve⊂tOr⊂aPaCityofRhipfcephRlussa71gZcusandDerCenIorvartqbiIisfor ameri⊂anisolatesofβ0esiagmiSubmittedtoxpApplAcarolE
Yonamine′HIthikiHHamakawaM′ShimabukurDTSugiyamaMlIsoda M1984StudiesoncaninebabesiosisinOkinawaIsland7pnVetScf46511 518N
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