Parasites & Vectors _ Full Text _ Prevalence and Zoonotic Potential of Canine Hookworms in Malaysia

6/3/2015 Parasites&Vectors|Fulltext|PrevalenceandzoonoticpotentialofcaninehookwormsinMalaysia

http://www.parasitesandvectors.com/content/5/1/88 1/6

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Abstract

BackgroundCaninehookworminfectionisendemicinSoutheastAsiancountrieswithaprevalencerangingfrom70%to100%,withzoonotictransmissionrepresentingapotentiallysignificantpublichealthconcern.However,therearelimiteddataavailableontheprevalenceofcaninehookwormsinMalaysia.ThisstudywasconductedtodeterminetheprevalenceofhookwormandAncylostomaspeciesamongdogsinMalaysia.

MethodsFaecalsampleswerecollectedfrom221dogslivinginurbanareas,ruralareasandanimalsheltersinSelangor.Faecalsampleswereprocessedusingtheformaletherconcentrationtechniquefollowedbywetmountpreparationandiodinestainingforthedetectionofhookwormeggs.SamplespositiveforhookwormeggswereexaminedusingPCR,targetingITS2and28srRNAregion,andsubsequentlysequencedinbothdirections.ThesequenceswerephylogeneticallyanalysedusingMrBayesforBayesianInference.

ResultsTheoverallprevalenceofhookwormamongdogswas48%(95%CI41.4154.95).Ruralstraydogshadthehighestprevalence71.4%(95%CI61.1381.49)followedbyurbanstraydogs,recording48%(95%CI34.1561.85)andlastlydogsinshelterswith28.7%(95%CI19.5637.84).Logisticregressionidentifiedruralstraydogsasahighriskgroup(OR=4.55,95%2.508.31)andkeepingdogsinsheltersasaprotectivefactor(OR=0.24,95%0.140.43).MolecularmethodsidentifiedbothAncylostomaceylanicumandAncylostomacaninumwithA.ceylanicumbeingpredominantamongurbanstraydogs.RuraldogshadahigherprevalenceofA.caninumthanA.ceylanicum,whilebothspeciesshowedequaldistributionamongdogsinshelters.PhylogeneticanalysisplacedA.ceylanicumisolatedfromdogsinonegroupwithA.ceylanicumhumanisolates.

ConclusionThisstudyindicatesthatdogshavethepotentialtoactasreservoirhostsofhumanhookworminfectioninMalaysia.Thisfindingnecessitatestheinclusionofdogsinanyinterventionstocombathookworminthecountry.

Keywords:HookwormDogsA.ceylanicumA.caninumMalaysia

Background

CaninehookworminfectionisendemicinSoutheastAsiancountrieswithaprevalencerangingfrom70%to100%,withzoonotictransmissionrepresentingapotentiallysignificantpublichealthconcern[13].DoghookwormsincludeAncylostomacaninumAncylostomabrazilienseAncylostomaceylanicumandUncinariastenocephala.Ofthesespecies,onlyA.ceylanicumdevelopstoadultinhumans,causingpatententerichookworminfection[4,5].Ontheotherhand,A.caninum,occasionallyreachesadulthoodinhumans,causingeosinophilicenteritis[68].

AlthoughA.brazilienseisthepredominantspecieswhichcauseshookwormrelatedcutaneouslarvamigrans(CLM),thelatelarvalstageofA.caninumhasbeenimplicatedinCLM[9],leadingtothelessercommonfolliculardermatitis[1012].Caninumlarvalstagehasalsobeensuspectedasacauseofdiffuseunilateral

Win500ofAmazonvouchersbycompletingour5minutesurvey Takethesurvey

Research

PrevalenceandzoonoticpotentialofcaninehookwormsinMalaysiaMohammedAKMahdy12*,YvonneALLim1,RomanoNgui1,MRSitiFatimah1,SeowHChoy1,NanJYap1,HeshamMAlMekhlafi12,JamaiahIbrahim1

andJohariSurin1

Parasites&Vectors2012,5:88 doi:10.1186/17563305588

Theelectronicversionofthisarticleisthecompleteoneandcanbefoundonlineat:http://www.parasitesandvectors.com/content/5/1/88

Received: 8March2012Accepted: 7May2012Published: 7May2012

2012Mahdyetal.licenseeBioMedCentralLtd.

ThisisanOpenAccessarticledistributedunderthetermsoftheCreativeCommonsAttributionLicense(http://creativecommons.org/licenses/by/2.0),whichpermitsunrestricteduse,distribution,andreproductioninanymedium,providedtheoriginalworkisproperlycited.

Correspondingauthor:MohammedAKMahdy

DepartmentofParasitology,FacultyofMedicine,UniversityofMalaya,50603KualaLumpur,Malaysia

DepartmentofParasitology,FacultyofMedicine,SanaaUniversity,Sanaa,Yemen

Email:[email protected]@[email protected]@[email protected][email protected]@yahoo.comJamaiahIbrahimjamaiahibrahim@[email protected]

* [email protected]

1

2



Figure1.Mapofthesamplingareas.

Figure2.AphylogenetictreebasedonpartialITS2sequencesofhookwormspeciesconstructedusingMrbayesprogram.Figuresonthebranchesarebootstrapprobabilities(in%)basedon1000bootstrappedtrees.AccessionnumbersindicatesequencesfromtheGeneBankdatabase.SequencesfromA.ceylanicuminfectinghumanswerereceivedfromapreviousstudyinMalaysia(Nguietal.,2012).

subacuteneuroretinitis[13]andhasbeenfoundintracellularlywithinmusclefibers[14].HookwormrelatedCLMcaseshavebeenreportedfromMalaysianpatients[1519]andintouristswhohavevisitedMalaysia[2022].

AlthoughhumanhookworminfectionsinMalaysiacontinuetocausesignificantmorbidity,particularlyamongdisadvantagedcommunities[2328],therearelimiteddataavailableontheprevalenceofcaninehookworms[2931].ArecentstudyamonghumanpopulationsusingmoleculartoolsshowedthatA.ceylanicumrepresented23.4%ofhumanhookworminfections.ThestudynotonlyisolatedA.ceylanicumfromhumansbutalsofromdogslivinginclosecontactwiththesehumansandstatisticalanalysisidentifiedcontactwithdogsandcatsasasignificantpredictorofhumanhookworminfections[32].Thepresentstudywillbeapplyingmoleculartoolsincombinationwithclassicalparasitologicalmethodstodeterminetheprevalenceandgeneticallycharacterizecaninehookwormfromdifferentlocations(i.e.,urbanareas,ruralareasandanimalshelters).Thisstudywillunfoldthepotentialroleofdogsaspossiblereservoirhostsofhumanhookworminfections.

Methods

SamplesandmicroscopyThestudywasconductedamongdogsfromthreedifferentlocations,whichincludedruralstraydogsinSelangorandPahang,urbanstraydogsfromKualaLumpuranddogsfromanimalsheltersinSelangor(Figure1). COMPARED tothestraydogsinruralandurbancommunities,dogsinanimalsheltersdoundergoperiodicdeworming.

Faecalsampleswerecollectedinwidemouthandscrewcappedfaecalcontainerswithattachedscoops,whichwereproperlylabelled.ThecollectedfaecalsamplesweretransportedtotheDepartmentofParasitology,FacultyofMedicine,UniversityofMalayaforfurtheranalysisinthesameday.Stoolsampleswereprocessedusingtheformalinetherconcentrationtechnique.Directwetmountwaspreparedbymixingasmallamount(approximately1gram)offaecesinadropofiodineonacleananddryslide.Thesmearwascoveredwithacoverslipandexaminedunderalightmicroscopestartingfrom LOWPOWER (10x)tohighpowermagnification(40x)forthepresenceofhookwormlikeeggs.

MolecularanalysisGenomicDNAwasextracteddirectlyfrompositivefaecalsampleusingPowerSoilDNAKit(MoBio,cat.no.12888100,CA,USA)accordingtomanufacturersinstructions.FinalelutionofDNAwasmadein50lofelutionbufferinsteadof200lasrecommendedbythemanufacturer.TheextractedDNAwasstoredat20CuntilrequiredforPCRamplification.

Apartialregion(310bp)ofinternaltranscribedspacerITS2and28SrRNAregionofAncylostomaspp.wasamplifiedusingaforwardprimerNC1(5ACGTCTGGTTCAGGGTTCTT3)andreverseprimerNC2(5TTAGTTTCTTTTCCTCCGCT3).ControlsampleswithoutDNA(negativecontrol/DNAblank)andwithhookwormgenomicDNA(positivecontrol)wereincludedineachPCRrun.ThePCRwascarriedoutina50lfinalPCRmixturecontaining1XPCRbuffer,200MdNTPs,1mMMgCl2,10pmolofeachprimer,5UTaqpolymeraseand6lofDNAtemplate.Thecyclingconditionswereasfollows:denaturationat94Cfor5min,

followedby30cyclesof94Cfor30s(denaturing),55Cfor30s(annealing),72Cfor30s(extension)andafinalextensionat72Cfor7min.PCRproductsweresubjectedforelectrophoresison1.2%agarosegelandstainedwithCybersafestain.

TheampliconswerepurifiedusingQIAquickGelExtractionKit(QIAgen,cat.no.28104,Hilden,Germany)accordingtothemanufacturersinstructions.AllthepurifiedampliconsweresentforDNAsequencinginbothdirectionsusingforwardandreverseprimerswithanABI3730XLsequencer(BioneerCorporation,SouthKorea).SequencechromatogramswereviewedusingSequenceScannerversion1.0programme(AppliedBiosystems,USA).Forwardandreversesequenceswereedited,manuallyalignedandtheconsensussequencewascreatedforeachsampleusingtheBioEditSequenceAlignmentEditorProgramme(http://www.mbio.ncsu.edu webcite ).ThesimilaritybetweeneachconsensussequencewasthencomparedtopreviouslypublishedsequencesofhookwormusingtheBasicLocalAlignmentSearchTool(BLAST)(http://blast.ncbi.nlm.nih.gov webcite ).SequencesgeneratedinthisstudyweredepositedinGenBank,undertheaccessionnumbers(JQ673419JQ673426).PhylogeneticanalysiswascarriedoutbyBayesianInferenceusingMonteCarloMarkovChain(MCMC)inMrBayes3.1.2[33].TheGeneralTimeReversible(GTR)modelofevolutionwasusedfornucleotidesubstitution[34]withgammadistributionrate.Referencesequencesfrompreviouspublishedstudieswereselectedforphylogeneticanalysis(Figure2).Thepercentageofreplicatetreesinwhichtheassociatedhookwormisolateswereclusteredtogetherinthebootstraptestvalues(1000replicates)isshownnexttothebranches.

StatisticalanalysisDatawereanalyzedusingSPSSprogrammedforwindowsversion11.5(SPSSInc.,Chicago.IL,USA).Univariateandmultivariateanalysisusinglogisticregressionwereappliedtoidentifyriskfactors.Chisquarewasusedtoinvestigatetheassociationbetweenvariables.Thesignificancewasdefinedasp



dogs.Theoverallprevalenceofhookwormthroughmicroscopydetectionwas48%(95%CI41.4154.95).Theprevalencewasthehighestamongruralstraydogs(71.4%,95%CI61.1381.49)followedbyurbanstraydogs(48%,95%CI34.1561.85)andfinallydogsinshelters(28.7%,95%CI19.5637.84)(Table1).Multivariateanalysisshowedthatruralstraydogsareatafivefoldhigherriskofhookworminfectioncomparedtodogslivinginotherlocations(OR=4.55,95%2.508.31).Keepingdogsinsheltersappearedtobeaprotectivefactor(OR=0.24,95%0.140.43)(Table2).

Table1.Prevalenceofhookworminfectionamongdogsaccordingtolocations

Table2.Univariateandmultivariateanalysisoftheassociationofhookwormwithlocations(n=221)

SpeciesidentificationanddistributionSpecimenspositiveforhookwormusingmicroscopy(106)weresubjectedtoPCRfollowedbyDNAsequencingbasedonapartialregion(310bp)ofITS2and28srRNAforspeciesidentification.Ofthese,82werePCRpositiveandsuccessfullysequenced.ComparisonofthesesequenceswithhookwormsequencesdepositedintheGenBankdatabaseusingBLASTshowedthat52%(43of82)wereA.ceylanicumand48%(39of82)wereA.caninum.ThestudyindictedthatA.ceylanicumwaspredominantamongurbanstraydogsandequallydistributedwithA.caninumindogslivinginshelters.Inruralcommunities,straydogswereinfectedmorewithA.caninumthanA.ceylanicum(Table3).

Table3.ThedistributionofAncylostomaspeciesamongdogsbasedonlocations

PhylogeneticanalysisSixteensequencesfromthisstudyrepresentingthethreegroupsofdogs(i.e.,dogsinshelters,urbanstrayandruralstraydogs)togetherwith8referencesequencesobtainedfromtheGenBankdatabaseand5sequencesrepresentingA.ceylanicumisolatedfromhumansinMalaysia[32]wereusedinthephylogeneticanalysisusingMrBayessoftwareforBayesianInference(Figure2).A.ceylanicumsequencesisolatedfromhumansanddogsweregroupedtogetherwithstrongsupport(0.97).A.caninumsequencesrepresentingthethreegroupsofdogswereplacedinoneclusterwith0.99bootstrapsupport.SequencesrepresentingA.duodenale,A.brazilienseandN.americanusweregroupedinseparatedclusters.

Discussion

Theoverallprevalenceofhookworminfectionsamongdogsbasedonsinglefaecalsamplingwas48%inthisstudywithruralstraydogshavingthehighestinfectionrate,followedbyurbanstraydogsandfinallydogsinshelters.ThesefindingsaresimilartoanotherpreviousstudycarriedoutamongdogsinruralandurbanareasinMalaysiainwhichtheprevalenceofhookworminfectionwas45%.However,inthepreviousstudybyAzianetal.[29],itwasfoundthaturbandogshadthehighestinfectionrateofhookworm.Thisstatementwasfurtherassuredbythehighercontaminationofsoilfromurbanareasinthesamestudy.Thisismostlikelyduetothepresenceofstraydogswhichscavengerubbishanddefecateallovertheplaces[29].

InThailand,theprevalenceofhookworminfectionbasedonmicroscopywas58.9%amongdogsintemplecommunities[2].InChina,66.3%ofdogsin175farmsinHeilongjiangProvincehadhookworminfections[35].InruralareasinIndia,theprevalenceofhookwormrangesfrom93%to98%[36,37].Thehighhookworminfectedstraydogsthatwanderanddefecateinthepublicareasincreasetheriskofcontaminationofstreets,publicparks,playgroundandbeacheswithhookwormlarvae.TheriskoftheenvironmentalcontaminationwasconfirmedbythedetectionofhookwormlarvaeofanimalorigininsandsamplesfromCaribbeanbeaches[38].ItwasalsofoundthatalltravelerswhovisitedNortheastBrazilhadacquiredhookwormrelatedCLMduringtheirstayatthebeaches[39].Furthermore,soilcontaminationwithhookwormlarvaecausedoutbreaksofCLMinkindergartens[40],publicparks[41],schools[42]andamongchildrenplayingwithsandboxes[43].

Multivariateanalysisindicatedthatruralstraydogsaremoreexposedtohookworminfectionandkeepingtheminsheltersprotectsthemfromtheinfection.Highratesamongruraldogscouldbeattributedtocontaminatedsoilintheruralareaswithhookwormlarvaeoffreeroamingdogsandcats.Soilcontaminationcouldalsobeaggravatedbypoorhumansanitationbehavior.Inaddition,thesoilinmostruralcommunitiesismuddyandmoistwhichfavoursthedevelopmentofhookwormlarvae[44].Thepresentstudyidentifiedthatkeepingdogsinsheltersreducesthatchanceofdogsacquiringhookworminfection,astheywillbelesslikelytobeexposedtotheinfectioncomparedtostraydogsandwillundergoregulardeworming.

Inthepresentstudy,bothA.ceylanicumandA.caninumhavebeenisolatedfromdogs.PhylogeneticanalysisusingsequencesofA.ceylanicumisolatedfromdogsandreferencesequencesofA.ceylanicumisolatedfromhumansplacedalldogsandhumanisolatesinonegroupwithhighbootstrapsupport(Figure2).ThisclusteringindicatesthatA.ceylanicummayplayapartinthetransmissionofhumanhookworminMalaysia.Duetotheinabilitytodifferentiatebetweenspeciescausinghumanhookwormbasedoneggmorphology,mostofthepreviousstudiescarriedoutinMalaysiadidnotidentifythespecies[2327].Thus,itislikelythatA.ceylanicumhasbeenoverlookedintheaetiologyofhumanhookworminMalaysia.

However,arecentstudybasedonmolecularmethods,conductedintheruralcommunityreportedA.ceylanicumasthesecondspeciescausinghumanhookworminfection[32].TheabilityofA.ceylanicumtoproducepatentinfectionsinhumanshasbeenreported[2,3,5,45,46].Inaddition,molecularstudyconductedinLaosshowedthatonethirdofhumanhookworminfectionsarecausedbyA.ceylanicumandthisspecieswasresponsiblefor85%ofhookworminfectionsamongdogs[3].ThedetectionofA.ceylanicuminhumansanddogswasalsoreportedinarecentstudyconductedinLaos[47].InasurveyconductedinThailand,A.ceylanicumwasrecordedasthepredominantspeciescausinghookwormindogsandwasdetectedinhumans.Inthesamestudy,onlyhumancasesinfectedwithA.ceylanicumsufferedchronicabdominaldisturbance[2].ThesereportsofA.ceylanicuminfectinghumansanddogsinthesamecommunityhighlighttheimportantroleofdogsinthenaturaltransmissionofhumanhookworminSoutheastAsiancountrieswhichwarrantfurtherinvestigations.Therefore,theroleofdogsinhumanhookwormtransmissionshouldbeconsideredduringtheimplementationofinterventionmeasurestocombatthedisease,suchas,masschemotherapywhichshouldbecombinedwithaproperdogmanagementprogrammeforeffectivecontrol.

Inthepresentstudy,A.caninumwasfoundin48%oftheinfecteddogs.ThisfindingisconcurrentwithreportsfromThailand[2],India[36]andAustralia[48].AncylostomacaninumcanestablishpathogenichumaninfectionsdependentonthemigrationofL3totheectopicsiteinthehumanhost.Ofthem,CLMisthemostcommonclinicalmanifestation[9].TherearelimitedreportsofCLMamonglocalpopulationsinMalaysia[1519].Yapfoundthatof31patientswithCLMreferredtoKualaLumpurgeneralhospital,only45.2%hadthecorrectdiagnosisbyreferredprimarycarephysicians[15].MissingthediagnosisofCLMforotherpruriticskinmanifestationmightunderestimatetheactualincidenceofCLM.AmongtravelersreturningfromMalaysia,CLMwasdiagnosedin13casesof42patientswithdermatologicdiagnosisintheperiodfrom1997to2006[20].However,itisnotclearwhichAncylostomaspeciescausedtheseCLMcases.HookwormrelatedCLMisusuallycausedbyA.brazilienseA.caninumA.tubaeformeandUncinariastenocephala[9,49].SincenoreportsofA.tubaeformeandU.stenocephalainMalaysiaandonlyonecaseofA.braziliensewasreportedtodate[32],weassumethatA.caninummightbethepotentialspecieswhichcausedthehookwormrelatedCLMinthiscountry.



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Conclusion

ThisstudyshowedhighprevalenceofhookwormamongdogsinMalaysiaespeciallyamongstraydogs.Thishighlightstheriskoftheseinfecteddogscontaminatingpublicareaswithhookwormlarvae.TheidentificationofA.ceylanicumindicatesthatdogsmayrepresentreservoirhostsofhumanhookwormsincethisspecieshasbeenconfirmedtocausepatentinfectioninhumanswhichwarrantfurtherstudiesonhumananddogsinthesamelocation.ThehighprevalenceofA.caninumshowsthatpeopleareatriskofgettinghookwormrelatedCLM,whichshouldbeconsideredinthediagnosisofpruriticskinmanifestations.DogsshouldbeconsideredasasignificantsourceofhumanhookworminfectioninMalaysiaandincludedintheparasitecontrolprogrammetominimizethesheddingofhookwormeggs.Itiscrucialthatpreventivemeasuressuchaspreventinganimalsfromdefecatinginthepublicareasandbeaches,cleaningupanimalwasteandeducatingpeopletowearprotectivefootwearwhiletheyareincontactwithsoilorsandybeachesbestrictlyimplementedespeciallyinpublicplaces.

Competinginterests

Theauthorsdeclarethattheyhavenocompetinginterests.

Authorscontributions

MAKM,YALLandJSdesignedthestudyMRSF,SHC,RNandNJYdidthefieldworkandthelabworkMAKMandHMAanalyzedthedataMAKMdraftedthemanuscriptMAKM,YALL,RN,HMAandJSrevisedthemanuscript.Allauthorshavereadandagreedwiththecontentofthesubmittedmanuscript.

Acknowledgments

TheauthorwouldliketothanktheanimalrefugeescentressuchasDBKL,SPCAandPAWSforgivinguspermissiontocollectthefaecalsamplesfromcanines.ThestudywassupportedbyUniversityofMalayaResearchGrant(RG02209SUS)andUniversityofMalayaHighImpactResearchGrant(J0000073587).

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