ht t p : / / w w w . b j m i c r o b i o l . c o m . b r /
Veterinary
Microbiology
Detection
of
seasonal
asymptomatic
dermatophytes
in
Van
cats
Ziya
Ilhan
a,∗,
Mehmet
Karaca
b,
Ismail
Hakki
Ekin
a,
Hasan
Solmaz
c,
Hasan
Altan
Akkan
b,
Mehmet
Tutuncu
daYuzuncuYılUniversity,FacultyofVeterinaryMedicine,DepartmentofMicrobiology,65080Van,Turkey bYuzuncuYılUniversity,FacultyofVeterinaryMedicine,DepartmentofInternalMedicine,65080Van,Turkey cYuzuncuYılUniversity,FacultyofPharmacy,DepartmentofPharmaceuticalMicrobiology,65080Van,Turkey dOndokuzMayısUniversity,FacultyofVeterinaryMedicine,DepartmentofInternalMedicine,55270Samsun,Turkey
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Articlehistory:
Received19February2015 Accepted11August2015
AssociateEditor:KarenSpadari Ferreira Keywords: Carriage Dermatophytes Isolation Vancat
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TheVancatisadomesticlandracefoundintheVanprovinceofeasternTurkey.Inthisstudy, weaimedtodeterminetheseasonalcarriageofdermatophytesinVancatswithout clini-callesions.Atotalof264hairspecimenswerecollectedfromclinicallyhealthycatsinand aroundtheVanProvince.Ofthesesamples,30.3%wereobtainedinspring,30.6%insummer, 16.6%inautumn,and22.3%inwinter;45.1%ofsampleswerefrommalecatsandtherest fromfemaleones.Ofthestudiedcats,118wereyoungerthan1year,78were1–3yearsold, and68wereolderthan3years.Thespecimensweresubjectedtodirectmicroscopic exam-inationwith15%potassiumhydroxideandculturedonSabourauddextroseagarand der-matophytetestmediumsupplementedwithcycloheximideandchloramphenicol. Dermato-phyteidentificationwascarriedoutbasedonmacroscopicandmicroscopiccolony morphol-ogy,ureaseactivities,invitrohairperforationtest,growthat37◦C,andpigmentationoncorn mealagar.Dermatophyteswereisolatedfrom19(7.1%)ofthe264specimensexamined.The mostfrequentlyisolatedfungiwereTrichophytonterrestre(4.1%),followedbyMicrosporum gyp-seum(1.1%),M.nanum(1.1%),andT.mentagrophytes(0.7%),andthesefungimayrepresenta healthriskforhumansincontactwithclinicallyhealthyVancats.M.caniswasnotisolated fromanyofthespecimens.Ourresultsshownosignificant(p>0.05)associationbetween car-riageofdermatophytesandthegenderofcats.Thecarriagerateofdermatophyteswashigh inspringandwinter,andtheonlypossibleriskfactorforinfectionwasageoftheanimal.
©2015SociedadeBrasileiradeMicrobiologia.PublishedbyElsevierEditoraLtda.Thisis anopenaccessarticleundertheCCBY-NC-NDlicense
(http://creativecommons.org/licenses/by-nc-nd/4.0/).
Introduction
TheVancatoriginatesfrom theEastern Anatoliaregionof Turkey,andshouldnotbeconfusedwiththeTurkishAngora
∗ Correspondingauthorat:YuzuncuYılUniversity,FacultyofVeterinaryMedicine,DepartmentofMicrobiology,65080Kampus/Van,Turkey.
E-mail:zilhan@yyu.edu.tr(Z.Ilhan).
cat.OneofthecharacteristicfeaturesoftheVancatiseyecolor andisaccordinglyclassifiedintothreegroups:botheyesblue; botheyesamber(yellowanditstones);andoneeyeblueand the otheramber(dischromatopsy).Blue-eyedVan cats usu-ally displayturquoise blue, whileambereyecolor displays
http://dx.doi.org/10.1016/j.bjm.2015.11.027
1517-8382/©2015SociedadeBrasileiradeMicrobiologia.PublishedbyElsevierEditoraLtda.ThisisanopenaccessarticleundertheCC BY-NC-NDlicense(http://creativecommons.org/licenses/by-nc-nd/4.0/).
tonalvariationsuchasamber,lightamber,yellow,andgreen almond.Althoughveryrare,browneyecolorcanalsobeseen. Vancatslovetoswimandplaywithwater,andaretheonlycat speciestodoso.Thiscatisasemi-long-hairedbreedthat con-venientlyshedsitshairduringthespringandsummeronlyto bereplacedbyashortvelvetycoat.Europeanshavebeen intro-ducingtheVancattotherestoftheworldsincethe1950s.1–3
Dermatophytosis(ringworm)isaninfectionofkeratinized structures,suchasnails,hair,andthe stratumcorneumof the skin, and is the most common fungal disease found inanimals.4 Dermatophytesare fungithat cause
dermato-phytosisand areclassifiedinthreegenera:Trichophyton(T.),
Microsporum (M.),and Epidermophyton (E.).While onlyafew speciesbelong totheTrichophytongenus, thereare approxi-mately40acceptedspeciesinthegenusEpidermophyton;and the Microsporum species usually cause dermatophytosis in domestic animals. Dermatophytes are usually divided into threeecologicalgroupsdependingontheirmainnaturalhost orhabitatasanthropophilic(humans),zoophilic(animals),or geophilic(soil).5–7
Asitsnamesuggests,felinedermatophytosisisan infec-tionofthesuperficialkeratinizedtissuesincats,anditsmost commoncauseisM.canisfungus.Twootherspecies,M. gyp-seumandT.mentagrophytes,canalsocausedermatophytosis inthecat,albeitwithalowerincidence.6,8,9M.canisinfections
incatsareofmajorimportanceascatsserveasareservoir ofthiszoonosis,whichisconsideredhighlycontagiousand potentiallypathogenicinhumans,especiallychildren.10
Der-matophytetransmissionoccursupon contactwithinfected hairorfomites(clippers,brushes),orfromtheenvironment (sporesinsoil),andinruralareas,up to80% ofall human fungalskininfectionsmaybeofanimalorigin.11
Itisimportanttonotethat canineand feline ringworm infections differ clinically. Canine infections generally pro-ducelesions, whereasclinical signs may notbeevident in cats,anditispossibletoculturedermatophytesfrom clini-callyhealthycatsthatactascarriersofconidiabut arenot themselves infected.6,12 While some reports on the
preva-lenceofdermatophyticfungiarebasedonsamplestakenonly fromanimalsshowingringwormlesions,13,14 othersstudies
usingrandompopulationsamplestakenfromanimalswith nolesionsrevealdifferentresults.15–17
Further,theincidenceofdermatophytosisisrelatedto geo-graphicregion, climate,and animal husbandrytechniques, and isfrequently found inyoung, stray, sick, or otherwise debilitatedanimals.4 Theasymptomaticcarrierstateisthe
mostimportantvariable inthetransmissionofthedisease amongcatsand fromcatstohumans.18 Tothebest ofour
knowledge, no previous studies have assessedthe asymp-tomaticcarrierstateinVancats.Therefore,theaimofthis study was to determinethe seasonal carriage of dermato-phytesinsuchpetswithoutovertclinicallesions.
Materials
and
methods
Geographicalcharacteristics
VanProvinceisthe18thlargestprovinceofTurkeyandliesin theEasternAnatoliaregionwithapopulationofover1million.
Itislocatedbetweennorthernlatitudesof38◦28 and east-ern longitudes of 43◦20, is 19,069km2 in area, and lies
between Lake Van and the Iranian border. This area faces extremesoftemperatureduringsummerandwinter,19,20has
adrycontinentalclimatewithcoolsnowywintersandwarm dry summers. Rainfall primarilyoccurs during spring and autumn,andannualaveragerainfallis384mm.Theregion’s averagemaximum temperatureduringwinterand summer are−2.2◦Cand20.4◦C,respectively,andtherelativehumidity
isapproximately59%.19
Samples
Atotalof264VancatsfromdifferentpartsoftheVanProvince, allofwhichwereownedandfedathome,wereselectedfor inclusion in the study. Complete body surface of the cats wasthoroughlyexaminedfordermatologicallesions,andonly thoseanimalsthatwerefreeofcutaneouslesions(Fig.1)and hadnotreceivedantifungaltherapyinthepreceding3months were includedinthestudy.Allcatsweredomesticatedand housedindoororincages.Aftercleaningthe selectedarea with70%alcohol,asterilebrushwasusedtotakehair sam-plesfrom thehead,neck,trunk,andtail. Eachsamplewas placedinaplasticstoragetubeandappropriatelylabeled.The sampleswerethentransferredtotheDepartmentof Microbi-ology,FacultyofVeterinaryMedicine,YuzuncuYılUniversity, Van,Turkey.
Ofthese264samples,80(30.3%)wereobtainedinspring, 81(30.6%)insummer,44(16.6%)inautumn,and59(22.3%)in winter;119(45.1%)werefrommalecatsand145(54.9%)were fromfemalecats.Atotalof118(44.7%)catswereyoungerthan 1year,78(29.5%)were1–3yearsold,and68(25.7%)wereolder than3years.
Cultureandidentification
Eachsamplewasdividedintotwoportions,oneportionwas usedfordirectmicroscopicexaminationandthe otherwas used for culture. Direct microscopic examinationwas per-formedafterthesamplewasplacedonaslideand30Lof 15%potassiumhydroxide(KOH)added.After5min.,thewet preparationwascarefullyexaminedunderbothlow(10×)and
Fig.2–Trichophytonterrestre.Sabourauddextroseagar
(left),dermatophytetestmedium(right),cornmealagar
(bottom),25◦C,7days.Surfaceofcolony.
high(40×)powerobjectives toobserve thefungalelements anddiagnosticmorphology.
The samples were cultured on Sabouraud dextrose agar (SDA; DM200, Mast Diagnostics, Merseyside, UK) and dermatophytetestmedium(DTM;7265A,Acumedia, Michi-gan,USA)supplementedwithchloramphenicol(0.05mg/mL; 220551,Calbiochem,Darmstadt,Germany)andcycloheximide (0.5mg/mL;C7698,Sigma-Aldrich,Steinheim,Germany).Petri disheswereincubatedat25◦Cfor5weeks.Theisolateswere examinedmacroscopicallyandmicroscopicallyafterstaining withlactophenolcottonblue(LFPM;1.13741,Merck,Germany) wetmounttechnique.Dermatophytespecieswereidentified based on grossand microscopic morphology (Figs. 2–4).In addition,pigmentproductiononcornmealagar(CMA;7350A, Acumedia,Michigan,USA),andureaseactivityonureaagar base (CM52; Oxoid, Basingstoke, UK), and growth at 37◦C on SDA were assessed, apartfrom in vitro hairperforation tests.5,7,21,22
Alldatawere analyzedusingtheMINITABver. 17demo statisticalanalysissoftwareforWindows.Resultswere con-sideredstatisticallysignificantatp<0.05or0.01.
Results
Dermatophyteswereisolatedfrom19ofthe264(7.1%) sam-ples.Themostfrequentlyisolatedfungiwere:T.terrestre(4.1%),
Fig.3–Trichophytonterrestre.Sabourauddextroseagar
(left),dermatophytetestmedium(right),cornmealagar
(bottom),25◦C,7days.Reverseofcolony.
Fig.4–Positiveinvitrohairperforationtest(Trichophyton
terrestre).
followedbyM.gypseum(1.1%),M.nanum(1.1%),andT. men-tagrophytes (0.7%). M. canis was not isolated from clinically healthy Van cats, and T. terrestre was the most commonly (57.8%)isolatedspeciesacrossallseasons(Tables1and2).In addition, somesaprophyticfungi(Alternariaspp., Chrysospo-rium spp., Ulocladium spp., Fusarium spp., Mucor spp., and
Penicilliumspp.)werealsoisolated.Nostatisticallysignificant (p>0.05)associationwasfoundbetweencarriageof dermato-phytesandgender.
Discussion
Dermatophytosis constitutes a major public health prob-lem in several countries and the most common factors affectingthedistributionandtransmissionofdermatophyte infectionsareanimalcontact,generalhygiene,andclimatic conditions.6,11,14,23Informationontheasymptomaticcarriage
ofdermatophytesinpetsisimportantforreducinghuman transmissionofzoophilicfungalinfections.Astudytodetect dermatophytecarriageindogs,conductedinAdana,Turkey, statedthatadetailedsurveyofkeratinophilicfungi,with par-ticularemphasisoncats,wasrequiredtopreciselydetermine dermatophytemicrobiota.16Therefore,theaimofthecurrent
studywastodeterminetheprevalenceandseasonalcarriage ofdermatophytesamongVancatswithoutclinicallesions.
The Van cathasa semi-long-haired coat thatis conve-niently shedduringspringand summer,andreplacedbya shortvelvetycoat.3Thesecatsaremuchlovedbythepeople,
Table1–Dermatophytespeciesisolatedfrom
asymptomaticVancats.
Dermatophytespecies Cats(n:264)
Culture Positive Negative 19(7.1%) 245(92.9%) Trichophytonterrestre 11(4.1%) Microsporumgypseum 3(1.1%) Microsporumnanum 3(1.1%) Trichophytonmentagrophytes 2(0.7%)
Table2–PrevalenceofdermatophytesisolatedfromthehairsamplesofasymptomaticVancatsaccordingtoseason,
age,andgender.
T.terrestre M.gypseum M.nanum T.mentagrophytes
Season Spring 5/80(6.2%) 2/80(2.5%) 2/81(2.4%) 2/80(2.5%) Summer 1/81(1.2%) – – – Fall 1/44(2.2%) – – – Winter 4/59(6.7%) 1/59(1.6%) 1/59(1.6%) – Age <1years 5/118(4.2%) 2/118(1.6%) 2/118(1.6%) 2/118(1.6%) 1–3years 3/78(3.8%) 1/78(1.2%) 0(0%) 0(0%) >3years 3/68(4.4%) 0(0%) 1/68(1.4%) 0(0%) Sex Female 7/145(4.8%) 2/145(1.3%) 3/145(2.1%) 1/145(0.6%) Male 4/119(3.3%) 1/119(0.8%) 0(0%) 1/119(0.8%)
especiallyintheVan Provinceand other regionsofTurkey, andaregenerallyfedinhomesbytheirowners.Asthesecats liveinclosecontactwithhumans,theymightbeapotential
hazard for human health if they passively carry
dermato-phyticfungi.Weisolatedmanyspeciesofdermatophytesfrom
asymptomaticcats,and theseanimalscouldbeconsidered
as sources ofsome geophilic (T. terrestre and M. gypseum), anthropophilic(T.mentagrophytes),andzoophilic(M.nanum) dermatophytes.Theseresultsindicatethataninfectedcatis probablyresponsibleforthedisseminationoffungalmaterial intoitsenvironmentanditsspreadtootheranimalsincontact withit.
Epidemiological studies on clinically healthy cats have
shownthatdermatophyteisolationratesrangebetween0.5% and 47.3%.15,24,25 In one study, M. gypseum (0.5%), T. men-tagrophytes (1.7%), and M. canis (47.3%)were cultured from asymptomatic stray cats.24 In another study, 100
asymp-tomatic stray cats from the north of Iran were examined to determine cutaneous fungal microbiota and this study isolated M. gypseum (3%) and T. mentagrophytes (1%), but no M. canis was isolated.25 Contrarily, Alpun and Ozgur15
reportedthatM.caniswasculturedin11%ofsamplesobtained fromclinicallyhealthycatsinIstanbul,Turkey.Weisolated pathogenicdermatophytes(M.nanum,M.gypseum,andT. men-tagrophytes)from clinicallyhealthy Vancats,whichconcurs withotherreportsontheprevalenceofT.mentagrophytesand
M.gypseum.24,25 Withrespecttothe prevalenceofM. canis,
theresultsofthepresent studyare incomplete agreement withthose of Shokohi and Naseri.25 Taken together, these
resultsindicatethattheprevalenceofdermatophytesvaries, anddependsonseason,temperature,andgeographicalarea.8 M.nanumisazoophilicspeciesthatismorecommoninpigs andisararecauseofringworminhumans.T.mentagrophytesis anotherzoophilicspeciesthatcaninfecthumans.Themajor animalhostsofM.nanumandT.mentagrophytesaredifferent petsandmammals.InAdana,Turkey,T.mentagrophytesisthe mostcommondermatophytespeciesisolatedfromthescalp ofasymptomatic children(carrierstate)andprobably indi-catesclosecontactwithasymptomaticpets,especiallycats anddogs.26Itisalsoimportanttoaddthatthesedermatophyte
speciesareusuallyacquireddirectlyfromthesoil,ratherthan fromanother host.However,the isolationofM.nanumand
T.mentagrophytesfromhealthy Vancatsisofinteresttopet
ownerswhomustbeinformedaboutpotentialdermatophyte infections,aswellastherisksassociatedwithacarrierstate.16 M. gypseum isa geophilicdermatophyte witha variable isolation ratefrom domesticanimals. Ranganathan etal.27
reportedafrequencyofisolationof8%from100healthycatsin India,whileothersurveysfromIranreported7.7%prevalence from differentanimals,including cats,28and3%prevalence
inasymptomatic straycats.29 Ofthe 130haircoatsamples
fromhealthywildcatsexaminedinanotherstudy,onlytwo (1.5%)werepositiveforM.gypseum.17AlthoughM.gypseumis
ageophilicdermatophyte,reportsfromJapan,30 Italy,31 and
Egypt,32 reaffirm theexistenceofthismold inhumanskin
lesions.Inthepresentstudy,three(1.1%)ofthe264samples showed presenceofM.gypseum, whichdenotesthe impor-tance ofVan catsas asymptomatic carriersand apossible sourceofhumaninfection.
M. canis is the majordermatophyte species that causes
TineacapitisinhumansandisprevalentinmostofEurope, Aus-tralia,SouthAmerica,andinpartsofAfrica.33Animalsoften
serveasthesourceofhumandermatophyticinfections,and catsareacceptedprincipalreservoirsofM.canis.8,9,13Indeed,
a study of111casesofhumandermatophytosis due toM. canisaccordingtotheiroriginofinfectionshowedthatitwas transmittedbycatsin91(81.9%)ofthecases.34Inaseparate
studytodeterminetheprevalenceandcarriageofM.canisin cats,samplesfrom632animalswereexaminedbycultureand byWood’slightexaminationwhichshowedacarriagerateof 2.1%.18Incontrast,wedidnotisolateM.canisfromtheVan
catsincludedinourstudy,andthisobservationconcurswith apreviousinvestigation.25OurfailuretoisolateM.canismay
eitherbeduetosmallnumberofsamplesevaluatedorbecause VancatsarenotnaturalreservoirsofM.canis.Tothebestofour knowledge,thisisthefirstreportdescribinginvestigationof dermatophytecarriageofVancats,butfurtherstudiesshould beconductedtodetermineotherdermatophytespeciesthat couldbeharboredbyasymptomaticVancats.
A varietyof studies havediscussed the seasonal distri-bution of dermatophyte species in cats.4,8,14 We report a
relatively highisolationrateinspringandwinter;however, nosignificant(p>0.05)associationwasfoundbetweenseason andisolationrate.
Some studies haveindicated that theage ofanimals is relatedtodermatophyteinfections,andthatyounganimals,
especiallythoseagedlessthanoneyear,aremoresusceptible to dermatophytosis.4,8,14,21 In accordance with these
find-ings,weshowanisolationrateof4.1%(11/264)fromanimals youngerthanoneyear,1.5%(4/264)fromthoseagedbetween 1and3yearsand,1.5%(4/264)fromcatsolderthan3years.
Severalprevious studies havenot observedany correla-tion between gender and dermatophyte infections in cats anddogs,8,14butCafarchiaetal.4statedthatmaledogswere
morefrequentlyaffectedbydermatophytosis.Inthepresent study,nosignificantassociationwasfoundbetweencarriage ofdermatophytesandthegenderofcats,eventhoughfemales showed ahigher isolation rate(4.9%, 13/264),compared to males(2.2%,6/264).Thiscouldberelatedtothehealthofthe cat,stressfactors,numberofspores,hygiene,andgenetic pre-disposition.
Ofthesaprophyticfungiisolated,Alternariaspp., Chrysospo-riumspp.,Ulocladiumspp.,Fusariumspp.,andMucorspp.,are commontomanyenvironments;Aspergillusspp.maybefound infood,whilePenicilliumspp.maybefoundontheground22,35
and the cats could have acquired these saprophytes from thesesources.
In conclusion, dermatophyte species were found in 19 (7.1%)ofthe 264 Van catsincluded inthe study,but clini-callyhealthyVancatscannotbeconsideredasasignificant reservoir of M. canis. The isolation of T. terrestre, M. gyp-seum,M.nanum,andT.mentagrophytesclearlyindicatesthat Vancatsshouldbeconsideredasamajorsourceofhuman pathogenic dermatophytes, even if the animals are clini-callyasymptomatic.Inaddition,weobservednosignificant (p>0.05)associationbetweencarriageofdermatophytesand genderofVancats.Thecarriagerateofdermatophyteswas highinspringandwinter,andtheagemightbeariskfactor.
Conflicts
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Theauthorsdeclarenoconflictsofinterest.
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