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Occurrence of Borrelia sp. among Wild Living Invasive and Native Mesocarnivores in Poland

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Wild living mesocarnivores, both introduced and native species, are able to adapt well to peri-urban environments, facilitating cross-species pathogen transmission with domestic animals, and potentially humans. Individual tissue samples derived from 284 specimens of six carnivore species, i.e., raccoon, raccoon dog, red fox, European badger, pine marten and stone marten, were used for molecular investigations with the nested PCR method. The animals were sampled in the Ruszów Forest District (Poland). We aimed to examine the relative importance of the studied mesocarnivores as hosts of Borrelia spp. and investigated their role in this spirochaete’s transmission cycle. We also aimed to trace the reservoir competence of these invasive and native predators and borreliosis eco-epidemiology in the context of a dilution effect. The overall prevalence of Borrelia spp. in the tested carnivores was 8.8%. Almost all of the consensus sequences of the partial flaB gene shared identity with a sequence of specific Borrelia species, i.e., B. afzelii, B. garinii and B. burgdorferi. Our results suggest that raccoons may play a role as reservoir hosts for these spirochaetal bacteria. The role of invasive species seems to be worthy of further analysis with reference to the circulation of vector-borne pathogens as well as in the context of the “dilution effect” hypothesis.
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Animals2022,12,2829.https://doi.org/10.3390/ani12202829www.mdpi.com/journal/animals
Article
OccurrenceofBorreliasp.amongWildLivingInvasiveand
NativeMesocarnivoresinPoland
JoannaHildebrand
1
,KacperJurczyk
2
,MarcinPopiołek
1
,KatarzynaBuńkowskaGawlik
1

andAgnieszkaPerecMatysiak
1,
*
1
DepartmentofParasitology,FacultyofBiologicalSciences,UniversityofWrocław,51148Wrocław,Poland
2
DepartmentofTropicalMedicineandParasitology,MedicalUniversityofGdańsk,
M.SkłodowskiejCurie3a,80210Gdańsk,Poland
*Correspondence:agnieszka.perecmatysiak@uwr.edu.pl
SimpleSummary:Vertebratehosts,especiallywildlivinganimals,arepivotaltothecirculationand
maintenanceofBorreliaspp.MesocarnivoresareinvolvedinLymediseaseecologyinsylvaticand
suburbanecosystems.Inthisstudy,weaimedtoexaminetherelativeimportanceofsixmedium
sizedcarnivorespecies,raccoon,redfox,raccoondog,Europeanbadger,pinemartenandstone
marten,ashostsofBorreliaspp.andinvestigatedtheirroleinthisspirochaete’stransmissioncycle.
Wealsoaimedtotracethereservoircompetenceoftheseinvasiveandnativepredatorsandtheeco
epidemiologyofBorreliaspp.inthecontextofadilutioneffect.Inallexaminedcarnivorespecies,
theoccurrenceofBorreliawasrecorded,andtheresultssuggestthatraccoonsmayplayaroleas
reservoirhostsforthesespirochaetalbacteria.Theroleofinvasivespeciesseemstobeworthyof
furtheranalysiswithreferencetothecirculationofvectorbornepathogensaswellasinthecontext
ofthe“dilutioneffect”hypothesis.
Abstract:Wildlivingmesocarnivores,bothintroducedandnativespecies,areabletoadaptwellto
periurbanenvironments,facilitatingcrossspeciespathogentransmissionwithdomesticanimals,
andpotentiallyhumans.Individualtissuesamplesderivedfrom284specimensofsixcarnivore
species,i.e.,raccoon,raccoondog,redfox,Europeanbadger,pinemartenandstonemarten,were
usedformolecularinvestigationswiththenestedPCRmethod.Theanimalsweresampledinthe
RuszówForestDistrict(Poland).Weaimedtoexaminetherelativeimportanceofthestudied
mesocarnivoresashostsofBorreliaspp.andinvestigatedtheirroleinthisspirochaete’stransmission
cycle.Wealsoaimedtotracethereservoircompetenceoftheseinvasiveandnativepredatorsand
borreliosisecoepidemiologyinthecontextofadilutioneffect.TheoverallprevalenceofBorrelia
spp.inthetestedcarnivoreswas8.8%.AlmostalloftheconsensussequencesofthepartialflaBgene
sharedidentitywithasequenceofspecificBorreliaspecies,i.e.,B.afzelii,B.gariniiandB.burgdorferi.
Ourresultssuggestthatraccoonsmayplayaroleasreservoirhostsforthesespirochaetalbacteria.
Theroleofinvasivespeciesseemstobeworthyoffurtheranalysiswithreferencetothecirculation
ofvectorbornepathogensaswellasinthecontextofthe“dilutioneffect”hypothesis.
Keywords:Borrelia;wildlivingcarnivores;invasivespecies;zoonosis
1.Introduction
ThegenusBorreliacomprisesarthropodbornespirocheteswhicharepathogensof
humanandanimals.Vertebratehosts,especiallywildlivinganimals[1],arepivotaltothe
circulationandmaintenanceofBorreliaspp.Thelevelofcompetencevariesbetweenhosts,
withrodentsappearingtobeimportanthosts[2,3],whereas,e.g.,roedeer(Capreolus
capreolus)seemtobezooprophylacticor“dilution”hosts[4].Accordingtothedilution
effecthypothesis,diversehostcommunitiesinhibittheparasiteabundancethrough
variousmechanisms,suchasregulatingpopulationsofsusceptiblehostsorinterfering
Citation:Hildebrand,J.;Jurczyk,K.;
Popiołek,M.;BuńkowskaGawlik,K;
PerecMatysiak,A.Occurrenceof
Borreliasp.amongWildLiving
InvasiveandNativeMesocarnivores
inPoland.Animals2022,12,2829.
https://doi.org/10.3390/ani12202829
AcademicEditor:MariaLuisa
Menandro
Received:19August2022
Accepted:17October2022
Published:18October2022
Publisher’sNote:MDPIstays
neutralwithregardtojurisdictional
claimsinpublishedmapsand
institutionalaffiliations.
Copyright:©2022bytheauthors.
LicenseeMDPI,Basel,Switzerland.
Thisarticleisanopenaccessarticle
distributedunderthetermsand
conditionsoftheCreativeCommons
Attribution(CCBY)license
(https://creativecommons.org/license
s/by/4.0/).
Animals2022,12,28292of7
withparasitetransmission[5–7].Nevertheless,theroleofcarnivoresas hosts inBorrelia
spp.ecologyremainsunclear.Thecurrentknowledgeofthecomplexinteractionbetween
thisdiversepathogenanditsvectorsaswellasdifferentreservoirandnonreservoirhosts
isstillincomplete.
Mesocarnivoressuchasraccoon(Procyonlotor),redfox(Vulpesvulpes),raccoondog
(Nyctereutesprocyonoides),Europeanbadger(Melesmeles),pinemarten(Martesmartes)and
stonemarten(Martesfoina)serveashostsforseveraltickspecies[8–11]andtheir
significantinvolvementinLymediseaseecologyinsylvaticandsuburbanecosystemsis
likely.Thecastorbeantick(Ixodesricinus)isknownasoneofthemainvectorsofBorrelia
spp.inCentralEuropeandhasquiteoftenbeenfoundontheseanimals[12–14].
InPoland,raccoonsandraccoondogsareconsideredinvasiveandalienspecies[15].
Theymayintroducenewpathogenstotheenvironmentandmayserveaspotentialhosts
formanyinfectiousagentsimportanttodomesticanimalsandhumans.Someofthe
predatorshaveadirectimpactonthehostcompetence,e.g.,redfoxesreduce,byhunting,
populationsofrodents,beingoneofthemostnumerousreservoirsofBorreliaburgdorferi
s.l.[16].
Here,weaimedtoexaminetheimportanceofsixmediumsizednativeandinvasive
speciesofcarnivorehostsofBorreliaspp.withoverlappingrangesandtoinvestigatetheir
roleinthespirochaetetransmissioncycle. Wealsoaimedtocheckthereservoir
competenceofthesepredatorsandtostudytheborreliosisecoepidemiology.
2.MaterialsandMethods
2.1.SampleCollection
Atotalof586tissuesamples(ear,spleen,liver)derivedfrom284specimensofsix
carnivorespecies,i.e.,raccoon(n=51),raccoondog(n=50),redfox(n=50),European
badger(n=53),pinemarten(n=27)andstonemarten(n=53),wereusedformolecular
study(Table1).TheanimalsweresampledintheRuszówForestDistrict(Poland),inthe
westpartoftheLowerSilesianWilderness,beingthelargestlowlandforestcomplexin
Europeandtheuniquelocationofcooccurrenceofthenativeandinvasivecarnivore
speciesinEurope.Thetissuesamplesobtainedthroughcollaborationwithotherprojects
werecollectedmainlyduringapredatorcontroloperationcarriedoutasapartofthe
capercaillie(Tetraourogallus)reintroductionprogramintheLowerSilesianForest[17,18].
ThetissuesamplesweredeliveredtothelaboratoryoftheDepartmentofParasitology,
UniversityofWrocław,andstoredat−20°C.
Table1.Tissuesamplesofcarnivorehostsusedinthepresentstudy.
CarnivoreHost
TotalNo.of
TestedSamplesNo.ofSampleTypes
EarBiopsySpleen Liver
Procyonlotor153515151
Nyctereutesprocyonoides150505050
Vulpesvulpes150505050
Melesmeles5353‐
Martesmartes2727‐
Martesfoina5353‐
Total586284151151
Animals2022,12,28293of7
2.2.MolecularAnalyses
DNAwasextractedusingtheBioTraceDNAPurificationKit(EURx,Poland),
followingthemanufacturer’sinstructions.DNAconcentrationswereestimatedwitha
NanoDrop2000spectrophotometer(NanodropTechnologies,Wilmington,DE,USA).The
moleculardetectionofBorreliaspp.wasperformedinthreesteps,i.e.,(1)qPCRsonall
obtainedtissuesamplesofinvasive(raccoonandraccoondog)andnativespecies(red
fox);(2)nestedPCRstargetingtheflaBgeneonselectedsamplesofallcarnivorespecies
cooccurringinthestudyarea;(3)conventionalPCR targetingthe5S23SrDNAintergenic
spacerregiononpositivesamplesfortheflaBgene.
Firstly,qPCRwiththeospAgeneasamarkerandprimersandprobessuch as B
OspA_modF,BOspA_borASandBOspAmodPattowasapplied[19,20]. The qPCR was
performed on all tissue samples(ear,liverandspleen)obtainedfromraccoons,raccoondogs
andredfoxes.ThepresenceofBorreliaspp.DNAwasdeterminedbytheamplificationof
a600bpfragmentoftheflaBgeneinnestedPCR,withtwoprimersets:132f,905rand
220f,824r[21].AstheqPCRresultswereconfirmedbynestedPCRs,weperformedonly
nestedPCRsforothercooccurringcarnivorespeciessuchasbadgersandpineandstone
martens(mustelids).Inthelaststep,theflaBpositivesampleswerefurtherexamined
usingconventionalPCRassaysamplifyingpartsofthe5S23SrDNAintergenicspacer
region(IGS)withprimersIGS_AandIGS_B[22].Negativecontrolswithnucleasefree
distilledwateraswellaspositivecontrols(B.afzeliifromIxodesricinus)wereincludedin
eachPCRreaction.InthePCRs,wefollowedtheprotocolsdescribedintheabove
mentionedliterature.
AllnestedPCRpositiveampliconswerepurifiedusingExoBAP(EURx)and
sequencedinbothdirectionsbyMacrogen(Amsterdam,theNetherlands)withthe
primersusedforDNAamplification.ThenucleotidesequenceswereeditedusingDNA
BaserSequenceAssemblysoftware(HeracleBioSoft,Mioveni,Romania)andcompared
toeachotherandwithcorrespondingsequencesdepositedinGenBankusingtheBasic
LocalAlignmentSearchTool(BLAST)program(http://blast.ncbi.nlm.nih.gov/Blast.cgi,
accessedon30September2022).TherepresentativesequencesweredepositedinGenBank
underaccessionnumbersOP559180–OP559187.
3.Results
Thesamplesobtainedfromskin(ear),spleenandliverofraccoons,raccoondogsand
foxeswerecheckedforthepresenceofBorreliaDNAusingqPCRandnestedPCR(14vs.
16).Apartfromonecase,allpositivesampleswereobtainedforearisolates(16/151;
10.6%).Theonlyothersample,whichprovedtobepositiveintheqPCR,originatedfrom
raccoonliver.Followingtheresultsobtainedforraccoons,raccoondogsandfoxes,the
nestedPCRswasperformedforcooccurringmustelidsonly.Theoverallprevalenceof
Borreliaspp.Inalltestedcarnivoreswas8.8%,consideringskinsamples(25/284)(Table2),
andtheinfectionratesvariedsignificantlybetweenthesehostspecies.Almostall
consensussequencesofthepartialflaBgenewhichwereanalyzedwiththeBLASTmethod
revealedsharedidentitywithasequenceofspecificBorreliaspecies,i.e.,B.afzelii(23),B.
garinii(1)andB.burgdorferi(1)(Figure1).
Thehighestprevalence(23.5%)wasobservedforraccoons(12/51)ascomparedto
raccoondogsandredfoxeswithasinglepositivesample(prevalenceof2%each)(Table
2).ThemajorityofpositivesampleswereBorreliaafzelii(100%identitywith,e.g.,
CP018262,DQ016619,KF894068,KX646195),onesamplefromfoxwasidentifiedasB.
garinii(100%homologywithafewsequences,i.e.,KF894068,MF150061).
ThebadgersprovedtobemoresusceptibletoBorreliainfection.Of53testedskin
samples,eightwerepositive(15.1%),whileDNAofBorreliasp.wasfoundintwosamples
obtainedfrompinemarten(27tested,i.e.,7.4%)andonefromstonemarten(53tested,i.e.,
1.9%).TheBLASTanalysisofsevensequencesshowed100%similaritytoseveralBorrelia
afzeliisequences;onewas100%identicaltoaBorreliaburgdorferisequence(acc.no.
Animals2022,12,28294of7
KF836508)fromIxodesricinusfromPoland(LowerSilesia)and99.8%identicaltoother
sequences(KX646200,KR782218)fromI.ricinusfromPolandaswellasonesequence(acc.
no.CP077727)fromBelarus.
TheinterspecificdivergenceofIGSsequencesofBorreliaafzeliiwas0.0–2.3%(0–6bp
outof264bp),andthreegroupscouldbedistinguishedwhenanalyzingthenucleotide
similarity.Thecomparisonbetweentheselinesandthehomologicalsequencesavailable
inGenBankshowed100%to99.2%similaritytosamplesderivedfromhumans(CP018262,
CP002933,JX888444),IxodesticksfromRussia,Estonia,Germany(CP009212,KX418638,
AY772053,MW489224,OL848283)aswellastosequencesobtainedfromrodenttissues
fromFranceandRomania(KY273112,KY123663).
Table2.Borreliaspeciesidentifiedinsamplesobtainedfromwildlivingmesocarnivoresbasedon
flaBgene.
CarnivoreHostNo.ofTested
Specimens
No.ofPositive
EarBiopsy
Samples
Prevalence(%)
(95%ConfidenceInterval)
DetectedBorreliaSpecies
(No.ofSequencedSamples)
Procyonlotor511223.5(15.9–33.1)Ba(12)
Nyctereutesprocyonoides5012.0(0.1–10.7)Ba(1)
Vulpesvulpes5012.0(0.1–10.7)Bg(1)
Melesmeles53815.1(8.8–23.8)Ba(7),Bb(1)
Martesmartes2727.4(1.3–23.7)Ba(2)
Martesfoina5311.9(0.2–7.4)Ba(1)
Total284258.8(6.3–12.2)Ba(23),Bb(1),Bg(1)
Ba—B.afzelii;Bb—B.burgdorferi;Bg—B.garinii.
Figure1.Distribution of Borreliaspecies identifiedinexaminedcarnivores.
4.Discussion
ThemajorityofdataonBorreliaspp.inraccoonsoriginatefromtheUSAandare
basedontheresultsofserologicaltesting[23–26].Additionally,theresultsofstudies
carriedoutbyTuftsetal.[27]showedthepresenceofB.burgdorferis.l.in2.6%ofexamined
samples.Serologicalstudiesconcerningthisspirochaetalinfectioninraccoonsfrom
introducedareas,carriedoutinJapan,revealedthepresenceofB.afzelii(0.1%)andB.
garinii(0.1%)[27,28].Ourresults,withthefirstmolecularevidenceofB.afzeliiinfection,
attaining24.0%intheEuropeanpopulationofintroducedraccoons,indicatethis
carnivoreasapotentialreservoirhostfortheaforementionedspirochaetalspecies.
Animals2022,12,28295of7
MolecularstudiescarriedoutbyWodeckaetal.[10]onEuropeanraccoondogsin
Polandrevealedthat11.9%oftestedanimalswerepositiveforB.garinii(dominant
species),followedbyB.afzeliiandB.valaisiana.Oursurveyindicatedamuchlowerlevel
ofBorreliainfection—2.0%inraccoondogs,beingdetectedasB.afzeliionly.Ontheother
hand,astudycarriedoutinSouthKorea,onnativecarnivores,resultedinthefirstreport
ofBorreliatheileri(0.7%)inraccoondogs[29].
Inthepresentstudy,badgersyieldedahigherprevalenceofBorreliaspp.(15.1%)
comparedtoothertestedspeciesofnativecarnivores,althoughBorreliaafzeliiandB.
burgdorferiweredetectedaswell.ResearchbyWodeckaetal.[10]providedevidencefor
Borreliainfectioninbadgerswithasimilarlevelofprevalence.AnalysesofallPCR
positiveblood,earbiopsyandliversamplesrevealedthat12%ofbadgerswereinfected
withborreliae.GernandSell[30]detectedthepresenceofbothB.afzeliiandB.valaisiana
in19.4%oftissuesamplesfromtheearsofbadgersinSwitzerland.ThePCRpositive
tissuesamplesidentifiedinbadgersrevealedthattheywereinfectedexclusivelywithB.
afzelii.Incontrast,duringresearchconductedinBelgiumandtheNetherlands,Borrelia
burgdorferi(s.l.)wasdetectedin0.9%ofliversamplesofEuropeanbadgers[11].
DNAofB.burgdorferi(s.l.)wasfoundintissuesofothermusteloidspecies,i.e.,stone
andpinemartens.Borreliaburgdorferi(s.l.)wasdetectedin3.9%ofspleensamplesofpine
martensand2.9%ofearbiopsiesofstonemartens[11].Tothebestofourknowledge,this
studyisthefirstmolecularidentificationofB.afzeliiinstonemarten(7.4%)andinpine
marten(1.9%).
Todate,therehavebeenonlyafewreportsfromEuropeontheoccurrenceofB.
burgdorferis.l.intissuesofredfoxesinGermany[31,32],Romania[33],Norway[34]and
Poland[35].ResultsofourstudyshowedthattheprevalenceofBorreliaspp.was2.0%and
B.gariniiwastheonlyspeciesdetectedinredfoxesinthissurvey.Borreliagariniiwasalso
solelynoticedinfoxesinGermany,buttherecordedprevalencewasmuchhigher—24%
[31].InPoland,theanalysisoftissuesof243animalsshowedthat23.5%ofthemcontained
DNAofBorreliaspp.,whereasB.gariniiwasidentifiedin91%oftheinfectedfoxes[35].
Ontheotherhand,onlyB.afzeliiandB.burgdorferiweredetectedintissuesofredfoxesin
Romania[33].
5.Conclusions
Tothebestofourknowledge,thisisoneof thefewandthemostcomprehensive
studiesundertakentoassesstheimportanceofintroducedandnativecarnivoresinthe
ecologyofBorreliaspp.worldwide.Inallexaminedcarnivorespecies,theoccurrenceof
Borreliawasrecorded.WeidentifiedB.afzelii(themostabundantgenospecies),B.garinii
andB.burgdorferiinstudiedanimals.ThehighestlevelofBorreliaprevalenceestimatedin
raccoonssuggeststheycanplayaroleasreservoirhostsforthesespirochaetalbacteria.
Thesignificanceofinvasivespeciesisworthfurtheranalysis,withspecialreferencetothe
circulationofvectorbornepathogensaswellasinthecontextofthe“dilutioneffect”
hypothesis.
AuthorContributions:Conceptualization,J.H.,A.PM.;methodology,J.H.,K.B.G.;material
collection,M.P.;molecularstudy,K.J.,K.BG.;resultsanalysis;J.H.,K.B.G.,A.PM.;writing—
originaldraftpreparation,J.H.,K.J.,K.B.G.,A.P.M.,writing—reviewandediting,J.H.,A.P.M.All
authorshavereadandagreedtothepublishedversionofthemanuscript.
Funding:TheresearchwaspartiallyfinancedbytheNationalScienceCentre,Poland,underthe
MINIATURA2project(grantno.2018/02/X/NZ6/01983).
InstitutionalReviewBoardStatement:TheapprovaloftheEthicsCommitteewasnotrequired
becausethematerialfortheresearchwasobtainedfromthepredatorcontroloperation.
InformedConsentStatement:Not applicable
DataAvailabilityStatement:Thedatapresentedinthisstudyareavailableonrequestfromthe
correspondingauthor.
Animals2022,12,28296of7
Acknowledgments:Thecarnivores’carcasseswerecollectedduringthepredatorcontroloperation
conductedasapartoftheprogramtoreintroducethecapercaillie(Tetraourogallus)intheLower
SilesianForest,financedbytheEuropeanCommission,theNationalFundforEnvironmental
ProtectionandWaterManagementandthePolishStateForests(grantLIFE11NAT/PL/428).Weare
gratefultoJanuszKobielski,HeadoftheRuszówForestDistrict,andDorotaMertafortheirhelpin
collectingthematerial.
ConflictsofInterest:Theauthorsdeclarenoconflictofinterest.
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... In Poland, different Borreliella spp. were identified in both raccoon dogs and raccoons [38,51]. In one study, B. garinii was found to be most frequent species detected in raccoon dogs, followed by B. afzelii; both pathogens are described as the dominant spirochetes found in ticks in Europe [38]. ...
... In one study, B. garinii was found to be most frequent species detected in raccoon dogs, followed by B. afzelii; both pathogens are described as the dominant spirochetes found in ticks in Europe [38]. In the second study, B. afzelii was the only species found in both, raccoon dogs and raccoons, with prevalences of 2.0% and 23.5%, respectively [51]. In our study, one raccoon dog and one raccoon were positive for Borreliella spp., which could be identified as B. afzelii in the raccoon. ...
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Raccoon dogs (Nyctereutes procyonoides) and raccoons (Procyon lotor) are invasive alien species originating from East Asia and North America, respectively. They are discussed as vectors and reservoirs for various infectious diseases, including vector-borne and zoonotic pathogens, and are therefore a potential threat to human and domestic animal health, as well as to biodiversity and conservation. In the years 2021 and 2022, 110 raccoon dogs (Nyctereutes procyonoides) and 30 raccoons (Procyon lotor) were screened via qPCR for the presence of Leptospira spp., Rickettsia spp. and Borreliella spp. in the German federal state of Schleswig-Holstein as part of a health and risk assessment study. Borreliella spp. were confirmed in one raccoon dog and one raccoon, identified as Borreliella afzelii in the raccoon. Leptospira spp. were found in 21 (19.44%) raccoon dogs and 2 (6.90%) raccoons. In five raccoon dogs, Leptospira spp. were identified as Leptospira borgpetersenii, Leptospira kirschneri and Leptospira interrogans.
... [71], Borrelia spp. [128], Coxiella burnetii [129], Francisella tularensis [130], Mycobacterium spp. [21], Bartonella spp. ...
... In contrast to the limited data regarding TBRF in wild carnivores, the occurrence of Lyme borreliosis in those animals was more comprehensively studied, and evidence of infection with Borrelia burgdorferi, B. afzelii, and Borrelia garinii was demonstrated in several wild carnivore species, including the raccoon (Procyon lotor), red fox, raccoon dog (Nyctereutes procyonoides), European badger, pine marten (Martes martes), and stone marten (M. foina) [59]. Control and management programs aim to reduce infection rates of various infectious agents, including Lyme borreliosis, in wild carnivores through oral vaccination programs. ...
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The role of red fox, Vulpes vulpes, and its associated ticks in maintaining Borrelia burgdorferi sensu lato (s.l.) was studied. A total of 1583 ticks were removed from ears of 120 infested animals and were identified as species using a nested PCR targeting the ITS2 and coxI fragments of Ixodes DNA. Ixodes kaiseri prevailed (76%), followed by I. canisuga, I. ricinus, and I. hexagonus. In total, 32.4% of 943 ticks revealed Borrelia DNA and 10 species of B. burgdorferi s.l. complex were identified. Borrelia garinii and B. afzelii comprised 70% of all infections. The other eight species included B. americana, B. bissettiae, B. burgdorferi sensu stricto (s.s.), B. californiensis, B. carolinensis, B. lanei, B. spielmanii, and B. valaisiana. Analysis of tissues from 243 foxes showed that 23.5% were infected with B. burgdorferi s.l. Borrelia garinii was detected in 91% of the infected animals, including 31% of mixed infections with B. afzelii, the second most prevalent species, followed by B. spielmanii. The predominance of B. garinii in PCR-positive animals and infected larval ticks (38.1%), suggests that this spirochete and B. afzelii are preferentially associated with foxes. Although red foxes are exposed to a high diversity of B. burgdorferi s.l. species found in engorged Ixodes ticks, their reservoir competence for most of them appears to be low.
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The order Carnivora includes over 300 species that vary many orders of magnitude in size and inhabit all major biomes, from tropical rainforests to polar seas. The high diversity of carnivore parasites represents a source of potential emerging diseases of humans. Zoonotic risk from this group may be driven in part by exceptionally high functional diversity of host species in behavioral, physiological, and ecological traits. We review global macroecological patterns of zoonotic parasites within carnivores, and explore the traits of species that serve as hosts of zoonotic parasites. We synthesize theoretical and empirical research and suggest future work on the roles of carnivores as biotic multipliers, regulators, and sentinels of zoonotic disease as timely research frontiers.
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Borrelia burgdorferi sensu lato (s.l.) causes the most common tick-borne infection in Europe, with Germany being amongst the countries with the highest incidences in humans. This study aimed at (1) comparing infection rates of B. burgdorferi s.l. in questing Ixodes ricinus ticks from different habitat types in Southern Germany, (2) analysing genospecies distribution by habitat type, and (3) testing tissue and ticks from hosts for B. burgdorferi s.l. Questing ticks from urban, pasture, and natural habitats together with feeding ticks from cattle (pasture) and ticks and tissue samples from wild boars and roe deer (natural site) were tested by PCR and RFLP for species differentiation. B. burgdorferi s.l. was found in 29.8% questing adults and 15% nymphs. Prevalence was lower at the urban sites with occurrence of roe deer than where these were absent. Borrelia burgdorferi s.l. DNA was found in 4.8% ticks from roe deer, 6.3% from wild boar, and 7.8% from cattle. Six genospecies were identified in unfed ticks: Borrelia afzelii (48.6%), Borrelia burgdorferi sensu stricto (16%), Borrelia garinii (13.2%), Borrelia valaisiana (7.5%), Borrelia spielmanii (6.2%), and Borrelia bavariensis (0.9%). This study shows high infection levels and a great diversity of Borrelia in questing ticks. The presence of roe deer seems to reduce B. burgdorferi s.l. infection rates in tick populations.
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Background Distribution and biology of Pholeoixodes ticks is not very well understood. The goal of the study was to collect new data on the Pholeoixodes tick occurrence in Slovakia.Methods Tick infestation of red foxes in the regions of Košice, Prešov, Bratislava and Žilina was studied during the period 2017–2018. Ticks were collected from the fur of animals using tweezers and identified using appropriate keys. In total, 146 red foxes (Vulpes vulpes) were investigated.ResultsIn total, 39 (26.7%) of animals were found to be infected with ticks from five species. Pholeoixodes ticks were found on 13 (3.4%) of the foxes: Ixodes hexagonus (Leach, 1815) on 5 specimens (3.4%), in the Košice, Prešov and Žilina regions; I. crenulatus (Koch, 1844) on 8 specimens (5.5%) in the Prešov and Bratislava regions; Ixodes ricinus (Linnaeus, 1758) collected from 25 (17.2%) foxes in every locality; Dermacentor reticulatus (Fabricius, 1794) from 5 foxes (3.4%) in the Košice, Prešov and Žilina regions; Haemaphysalis concinna (Koch, 1844), from 4 foxes (2.8%) from the Košice region.Conclusions Ixodes hexagonus has been previously recorded in Slovakia. However, this is the first finding of I. crenulatus in the country. The morphological features of the I. crenulatus specimens found in Slovakia were identical to those of ticks described in Poland and descriptions given in identification keys.
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Borrelia burgdorferi sensu lato (Bbsl) is a bacterial species complex that includes the etiological agents of the most frequently reported vector-borne disease in the Northern hemisphere, Lyme borreliosis. It currently comprises > 20 named and proposed genospecies that use vertebrate hosts and tick vectors for transmission in the Americas and Eurasia. Host (and vector) associations influence geographic distribution and speciation in Bbsl, which is of particular relevance to human health. To target gaps in knowledge for future efforts to understand broad patterns of the Bbsl-tick-host system and how they relate to human health, the present review aims to give a comprehensive summary of the literature on host association in Bbsl. Of 465 papers consulted (404 after exclusion criteria were applied), 96 sought to experimentally establish reservoir competence of 143 vertebrate host species for Bbsl. We recognize xenodiagnosis as the strongest method used, however it is infrequent (20% of studies) probably due to difficulties in maintaining tick vectors and/or wild host species in the lab. Some well-established associations were not experimentally confirmed according to our definition (ex: Borrelia garinii, Ixodes uriae and sea birds). We conclude that our current knowledge on host association in Bbsl is mostly derived from a subset of host, vector and bacterial species involved, providing an incomplete knowledge of the physiology, ecology and evolutionary history of these interactions. More studies are needed on all host, vector and bacterial species globally involved with a focus on non-rodent hosts and Asian Bbsl complex species, especially with experimental research that uses xenodiagnosis and genomics to analyze existing host associations in different ecosystems.
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Haemaphysalis longicornis, the Asian longhorned tick, is an invasive ixodid tick that has rapidly spread across the northeastern and southeastern regions of the United States since first reported in 2017. The emergence of H. longicornis presents a potential threat for livestock, wildlife, and human health as the host associations and vector potential of this invasive pest in the United States are poorly understood. Previous field data from the United States has shown that H. longicornis was not associated with natural populations of small mammals or birds, but they show a preference for medium sized mammals in laboratory experiments. Therefore, medium and large sized mammals were sampled on Staten Island, New York, United States, to determine H. longicornis host associations and vector potential for a range of human and veterinary pathogens. A total of 97 hosts were sampled and five species of tick (Amblyomma americanum, Dermacentor variabilis, H. longicornis, Ixodes scapularis, Ixodes cookei) were found feeding concurrently on these hosts. Haemaphysalis longicornis was found in the highest proportions compared with other native tick species on raccoons (55.4%), Virginia opossums (28.9%), and white-tailed deer (11.5%). Tissue, blood, and engorged larvae were tested for 17 different pathogens using a nanoscale PCR platform. Infection with five pathogens (Borrelia burgdorferi, Anaplasma phagocytophilum, Rickettsia spp., Mycoplasma haemocanis, and Bartonella spp.) was detected in host samples, but no pathogens were found in any larval samples. These results suggest that although large and medium sized mammals feed large numbers of H. longicornis ticks in the environment, there is presently a low potential for H. longicornis to acquire pathogens from these wildlife hosts. Ó