Isolation of Microsporum canis from the hair coat of pet dogs and ...

Isolation of Microsporum canis from the hair coat ofBlackwell Publishing Ltdpet dogs and cats belonging to owners diagnosedwith M. canis tinea corporisClaudia Cafarchia*, Diana Romito*,Gioia Capelli†, Jacques Guillot‡ andDomenico Otranto**Dipartimento di Sanità e Benessere Animale, Facoltà di MedicinaVeterinaria, Strada Provinciale per Casamassima km 3, 70010Valenzano, Bari, Italy†Istituto Zooprofilattico Sperimentale delle Venezie, Legnaro-Padova‡Service de Parasitologie-Mycologie, Ecole Nationale Vétérinaired’Alfort, FranceCorrespondence: Otranto Domenico, Dipartimento di Sanitàe Benessere Animale, Facoltà di Medicina Veterinaria, Str. prov.leper Casamassima Km, 3, 70010, Valenzano, Bari, Italy.Tel: +39080 4679839; Fax: +39080 4679839;E-mail: d.otranto@veterinaria.uniba.itWhat is known about the topic of this paper• Microsporum canis is the most common dermatophytefound on dogs and cats.• It has also been frequently isolated in human casesof tinea capitis and tinea corporis.• The infection may be acquired from infected animalswith cutaneous lesions but also from asymptomaticcarriers or from the environment where infectivearthroconidia survive for a long time.What this paper adds to the field of veterinarydermatology• The present investigation studied the relationshipbetween the presence of dermatophytes in thehaircoats of dogs and cats without cutaneous lesionsand the occurrence of the disease in their respectiveowners.• It represents an important issue considering thatasymptomatic M. canis carriers are considered to bea critical factor in the epidemiology of dermatophytosisin humans.AbstractMicrosporum canis has been frequently isolated fromhuman cases of tinea capitis and tinea corporis. Theinfection may be acquired from infected animals withcutaneous lesions but also from asymptomatic carriersor from the environment. As asymptomatic M.canis carriers are considered to be a critical factor inthe epidemiology of dermatophytosis in humans, thisstudy investigated the relationship between the presenceof dermatophytes on the hair coats of dogs andcats without cutaneous lesions and the occurrence ofthe disease in their respective owners. A total of 136dogs and 248 cats were sampled from January 1999 toJanuary 2005. Seventy-eight animals (22 dogs and 56cats) belonged to individuals affected by tinea corporiscaused by M. canis and 306 (114 dogs and 192 cats) toindividuals without dermatophytosis. Age, sex, breed,habitat and season were recorded for each animal andexamined as potential risk factors. Dermatophyteswere isolated from 20.5% of the dogs and 28.2% ofthe cats. Microsporum canis was isolated from 36.4%of dogs cohabiting with owners diagnosed with tineacorporis but it was never isolated from dogs whoseowners had no lesions. By contrast, M. canis wasisolated from 53.6% of cats cohabiting with ownersdiagnosed with tinea corporis and from 14.6% ofcats whose owners had no signs of the disease. Theseresults clearly indicate that both cats and dogs shouldbe considered as a major source of pathogenic dermatophytesfor humans even when they do not presentclinical signs of dermatophytosis.Accepted 14 June 2006IntroductionDermatophytosis is a common infection of keratinizedtissues (e.g. skin, nails and hair) characterized by multifocalalopecia, scaling and circular lesions. Microsporum andTrichophyton species are responsible for infections inanimals and Microsporum canis is the most commonlyisolated dermatophyte from dogs and cats with or withoutcutaneous lesions. 1–4 Microsporum gypseum, Trichophytonterrestre and Trichophyton ajelloi are geophilic dermatophytesmainly isolated from dogs and cats withoutlesions; 2,5 however, the pathogenic role of these geophilicspecies is still a matter of controversy. The transmissionof M. canis occurs via infective arthrospores present onthe hair coats of dogs and cats or in the environment. 1Humans may be infected, and M. canis has become themost frequently encountered zoonotic dermatophyte inurban areas. 6,7The prevalence of M. canis infections in humans differsfrom one country to another. 8 In Italy, it is the most commondermatophyte isolated from tinea capitis and tineacorporis cases. 9,10 This may be explained by the greatnumber of dogs and cats kept as pets in this country. 9–11Asymptomatic animal carriers of M. canis are consideredto be a critical factor in the epidemiology of the disease as50% of humans exposed to infected asymptomatic animals,especially cats, may become infected. 12 The preva-© 2006 The Authors. Journal compilation © 2006 European Society of Veterinary Dermatology. 17; 327–331 327

Pets as source of Microsporum canis infection to humansTable 3. Prevalence of Microsporum canis isolated from the hair coatof asymptomatic dogs and cats according to sex, age, breed, habitatand seasonDogsCatsSexFemale 4/80 (5.0%) 32/128 (25.0%)Male 4/56 (7.1%) 26/120 (21.7%)Age< 1 years 0/44 (0%) 26/82 (31.6%)1–5 years 4/48 (8.3%) 18/92 (19.5%)> 5 years 4/44 (9.1%) 14/74 (18.9%)BreedCross-breed 2/68 (2.9%) 26/94 (27.7%)Pure breed 6/68 (8.8%) 32/154 (20.8%)HabitatUrban 4/36 (11.1%) 4/98 (4.1%)Rural 4/100 (4.0%) 54/150 (36.0%)SeasonSpring 2/30 (6.6%) 18/116 (15.5%)Summer 4/28 (14.3%) 4/52 (7.7%)Fall 0/68 (0%) 21/53 (39.6%)Winter 2/10 (20.0%) 15/27 (55.6%)(OR = 4.233; CI = 1.956–9.160) proved to act as predisposingfactors for M. canis carriage in cats (P < 0.001),whereas age (OR = 2.503; CI = 1.204–5.202) and breed(OR = 3.208; CI = 1.496–6.878) were risk factors forgeophilic dermatophyte infections in dogs (P < 0.001). Inother words, cats living in a rural environment and those< 1 year of age sampled in the winter months were morelikely to carry M. canis, whereas no differences wereobserved according to sex or breed. Dogs < 1 year of ageand pure breed dogs showed a higher prevalence ofgeophilic species carriage than other dogs (Table 4). Nogeophilic dermatophytes were isolated from female catsor from cats older than 5 years nor were they isolated fromdogs or cats in the winter months.DiscussionThe role of cats as asymptomatic carriers of M. canis hasbeen extensively described by many investigatiors 8,20 andcats are now recognized as major sources of infectionto other animals and their owners. The role of cats inhuman infection may be related to the greater number ofspores shed in the environment by infected cats than thatshed by dogs. 12 The present study clearly indicated thatasymptomatic dogs could also carry pathogenic dermatophytes(M. canis and geophilic species) on their hair coats.Microsporum canis was more frequently isolated from thehair coats of dogs and cats cohabiting with owners diagnosedwith M. canis tinea corporis. However, it was alsopresent on the hair coat of some cats cohabiting withhealthy owners but they were never isolated from dogsliving with healthy owners. These results seem to indicatethat many dogs examined in the present study were notresponsible for the transmission of M. canis to humans,and suggest that cats were the source of transmissionof M. canis to humans. When M. canis was detectedon the coat of asymptomatic dogs, their owners consistentlyhad M. canis tinea corporis. However, when dogowners had dermatophytosis, the dogs were morefrequently culture negative (14 dogs) than culture positiveTable 4. Prevalence of geophilic dermatophyte species isolated fromthe hair coat of asymptomatic dogs and cats according to sex, age,breed, habit and seasonDogsCatsSexFemale 14/80 (17.5%) 0/128 (0%)Male 8/56 (14.2%) 10/120 (8.3%)Age*< 1 years 14/44 (31.8%) 4/82 (4.9%)1–5 years 4/48 (8.3%) 6/92 (6.5%)> 5 years 2/44 (4.5%) 0/74 (0%)BreedCross-breed 2/68 (2.9%) 6/94 (6.4%)Pure breed 20/68 (29.4%) 4/154 (2.6%)HabitatUrban 2/36 (5.5%) 2/150 (1.3%)Rural 20/100 (20.0%) 8/98 (8.2%)SeasonSpring 4/30 (13.3%) 6/116 (5.2%)Summer 6/28 (21.4%) 2/52 (3.8%)Fall 12/68 (17.6%) 2/53 (3.8%)Winter 0/10 (0%) 0/27 (0%)*Age has not been reported for two dogs and for two cats.(8 dogs). These results suggest that M. canis had beenacquired from a common source or had been transmittedfrom the owners to their dogs.The finding of culture-positive cats cohabiting with ownerswith no cutaneous lesions is also of interest. In particular,the fact that all of these cats, with the exception oftwo, lived in rural areas and had access to the outdoorsindicates that this lifestyle represents a risk factor forculture-positive status. The detection of M. canis in severalowners whose pets did not carry dermatophyte arthroconidiamay indicate that the infection occurred throughcontact with another animal or an environmental source.In the present study, age, habitat, and sampling periodwere predisposing factors for M. canis carriage in cats.The high prevalence of M. canis infection in younganimals has been extensively documented in previousinvestigations 3,13,14,21 while there is evidence that adultanimals and long-haired cats from catteries with endemicdermatophytosis are frequently asymptomatic carriers.22,23 In this study, cats younger than 1 year of age andcats sampled in the winter months carried M. canismore frequently than adult cats and cats sampled duringother seasons. It is possible that some of the young,culture-positive cats sampled during the winter eventuallydeveloped cutaneous lesions after the sampling date. Thishypothesis is supported by previous findings showing thatin the same area of southern Italy the highest prevalenceof M. canis carriage was in the winter months for dogs andcats, whereas skin lesions caused by dermatophytesoccurred in the summer and fall months. 3 Seasonalitymight play a relevant role on host receptivity and M. canispathogenicity, which may explain differences in prevalenceof dermatophyte isolation or infection according toseasons.Interestingly from an ecological standpoint, M. canisinfections are considered to be mycoses with an ‘urbancycle’ 3,24 and animals living in urbanized areas usuallydevelop lesions. 3 The present study showed a high prevalenceof M. canis carriage in cats living in rural areas and© 2006 The Authors. Journal compilation © 2006 European Society of Veterinary Dermatology. 329

Cafarchia et al.this may be explained by the presence of M. canis in wildanimals, 25,26 suggesting that most cats allowed to rangefreely are likely to increase their risk for infection.The high prevalence of geophilic dermatophytes on dogcoats may be explained by the warm climate of southernItaly which affects the viability of these species as well asthe susceptibility of the hosts. 3,15 Age and breed proved tobe predisposing factors for geophilic dermatophyte infectionsin dogs; however, the high prevalence of geophilicdermatophytes in pure breeds (e.g. German sheep dog,Italian Bracco) might be attributed to their lifestyle ratherthan to bred susceptibility factors. Almost half of theexamined pure breed dogs lived outdoors and geophilicdermatophytes were isolated only from these animals.Although the results did not attain statistical significance,the most frequent carriers of geophilic dermatophyteswere male cats younger than 5 years of age living in ruralareas. A likely explanation for this is that younger animals(dogs and cats), especially males, tend to live outdoors inrural areas, and contact with the soil exposes them to fungaltransmission from this source. 3,13,14 Geophilic dermatophytecarriage was high in the summer months for dogsand spring months for cats, whereas none of thesespecies was isolated in the winter months, in agreementwith previous findings. 3 In the winter months the frozenstate of the soil or the prolonged rainfalls and excessivemoisture of the soil may minimize the likelihood of closecontact between hosts and natural reservoir for infection. 15In summary, the results of this investigation demonstratedthat not only cats, but also dogs, living in SouthernItaly carry dermatophyte arthroconidia in their hair coatwhile remaining asymptomatic. The risk of M. canis transmissionto owners from asymptomatic cats was higherthan from asymptomatic dogs. Moreover, the factors influencingthe carrier role of pets were not the same for dogsand cats.References1. Sparkes AH, Werrett G, Stokes CR et al. Microsporum canis: inapparentcarriage by cats and the viability of arthrospores. Journalof Small Animal Practice 1994; 35: 397–401.2. Cabanes FJ, Abarca ML, Bragulat MR et al. Seasonal study offungal biota of the fur of dogs. Mycopathologia 1996; 133: 1–7.3. Cafarchia C, Romito D, Sasanelli M et al. The epidemiology ofcanine and feline dermatophytoses in southern Italy. Mycoses2004; 47: 508–13.4. Patel A, Lloyd DH, Lamport AI. Survey of dermatophytes on clinicallynormal cats in the southeast of England. The Journal ofSmall Animal Practice 2005; 46: 436–9.5. Moriello KA, DeBoer DJ. Fungal flora of the coat of pet cats.American Journal of Veterinary Research 1991; 52: 602–6.6. Lunder M, Lunder M. Is Microsporum canis about to become aserious dermatological problem? Dermatology 1992; 184: 87–9.7. 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Veterinary Record 1956;133: 57–61.14. Cabanes FJ, Abarca ML, Bragulat MR. Dermatophytes isolatedfrom domestic animals in Barcelona, Spain. Mycopathologia1997; 137: 107–13.15. Kaplan W, Ivens MS. Observations on the seasonal variationsin incidence of ringworm in dogs and cats in the United States.Sabouraudia 1961; 1: 91–102.16. MacKanzie DWR. The extra-human occurrence of Trichophytontonsurans var. sulfureum in a residential school. Sabouraudia1961; 1: 58–64.17. Rebell G, Taplin D. Dermatophytes. Their Recognition and Identification.Coral Gables, FL: University of Miami, 1974.18. de Hoog GS, Guarro J, Gene J et al. Atlas of Clinical Fungi, 2ndedn. Utrecht, The Netherlands: Centraalbureau voor Schimmelcultures,2000.19. Hosmer DW, Lemeshow S. Applied Logistic Regression, 2ndedn. New York: Wiley & Sons, 2000.20. Mignon BR, Losson BJ. Prevalence and characterization of Microsporumcanis carriage in cats. Journal of Medical and VeterinaryMycology 1997; 35: 249–56.21. Lewis DT, Foil CS, Hosgood G. Epidemiology and clinical featuresof dermatophytosis in dogs and cats at Louisiana State University.Veterinary Dermatology, 1991; 2: 53–8.22. Thomas MLE, Scheidt VJ, Walzer RL. Inapparent carriage ofMicrosporum canis in cats. Compendium on Continuing Educationfor the Practicing Veterinarian 1989; 5: 563–71.23. Moriello KA, DeBoer DJ. Fungal flora of the hair coat of cats withand without dermatophytosis. Journal of Medical and VeterinaryMycology 1991; 29: 285–92.24. Mantovani A, Battelli G, Zanetti R. Special problems of zoonosesconnected with urban areas. Annali Dell’istituto Superiore DiSanita 1978; 14: 287–93.25. Gallo MG, Lanfranchi P, Poglayen G et al. Seasonal 4-year investigationinto the role of the alpine marmot (Marmota marmota) asa carrier of zoophilic dermatophytes. Medical Mycology 2005; 43:373–9.26. Gallo MG, Tizzani P, Peano A et al. Eastern cottontail (Sylvilagusfloridanus) as carrier of dermatophyte fungi. Mycopathologia2005; 160: 163–6.Résumé Microsporum canis a fréquemment été isolé des cas tinea capitis et de tinea corporis chezl’homme. L’infection peut être acquise à partir d’un animal infecté avec des lésions cutanées, mais égalementà partir d’un porteur asymptomatique ou de l’environnement. Comme les porteurs asymptomatiquessont considérés critiques dans l’épidémiologie des dermatophytoses humaines, cette étude s’estintéressée à la relation entre la présence de dermatophytes sur le pelage de chiens et de chats sans lésioncutanée et l’apparition de lésions chez leurs propriétaires. Au total, 136 chiens et 248 chats ont été prélevésentre janvier 1999 et janvier 2005. Soixante dix huit animaux (22 chiens et 56 chats) appartenaient à des330 © 2006 The Authors. Journal compilation © 2006 European Society of Veterinary Dermatology.

Pets as source of Microsporum canis infection to humanspropriétaires souffrant de tinea corporis due à M. canis et 306 (114 chiens et 192 chats) à des propriétairessans dermatophytose. L’âge, le sexe, la race, l’habitat et la saison ont été étudiées pour chaque animal etexaminés comme risque potentiel. Des dermatophytes ont été isolés de 20.5% des chiens et 28.2% deschats. M. canis a été isolé de 36.4% des chiens cohabitant avec un propriétaire présentant une tinea corporismais jamais chez les chiens don’t les propriétaires ne présentaient pas de lésion. A l’opposé, M. canis aété isolé de 53.6% des chats cohabitant avec un propriétaire souffrant de tinea corporis et de 14.6% deschats dont le propriétaire ne présentait pas de lésion. Ces résultats indiquent clairement que chiens et chatsdoivent être considérés comme des sources majeures de dermatophytes pathogènes pour l’humain, mêmesans signe clinique de dermatophytose.Resumen Microsporum canis se ha aislado con frecuencia en casos humanos de tinea capitis y tineacorporis. La infección puede adquirirse de animales infectados y con lesiones cutáneas, pero también deportadores asintomáticos o del ambiente. Ya que los portadores asintomáticos de M. canis se consideranun factor crítico en la epidemiología de la dermatofitosis humana, en este estudio investigamos la relaciónentre la presencia de dermatofitos en el pelo de perros y gatos sin lesiones cutáneas, y la presencia de laenfermedad en los respectivos dueños. Se tomaron muestras de un total de 136 perros y 248 gatos entreEnero de 1999 y Enero del 2005. Setenta y ocho animales (22 perros y 56 gatos) pertenecieron a dueñosafectados con tinea corporis causada por M. canis y 306 (114 perros y 192 gatos) a individuos sin dermatofitosis.Edad, género, raza, habitat y estación se anotaron para cada animal y se examinaron como potencialesfactores de riesgo. Se aislaron dermatofitos de un 20.5% de los perros y de un 28.2% de los gatos. M. canisse aisló de un 36.4% de los perros conviviendo con dueños diagnosticados con tinea corporis, pero nuncase aisló en perros cuyos dueños no tenían lesiones. En contraste, M. canis se aisló de un 53.6% de gatosconviviendo con propietarios diagnosticados con tinea corporis y de un 14.6% de gatos cuyos propietariosno presentaron enfermedad. Estos resultados claramente demuestran que tanto perros como gatos debenser considerados una fuente importante de dermatofitos patógenos para humanos, incluso si no presentansignos clínicos de dermatofitosis.Zusammenfassung Microsporum canis wurde häufig bei humanen Fällen von Tinea capitis und Tineacorporis isoliert. Die Infektion kann von einem infizierten Tier mit Hautläsionen stammen, kann aberauch von asymptomatischen Trägern oder aus der Umgebung kommen. Da asymptomatische M. canisTräger als kritische Faktoren bei der Epidemiologie von Dermatophytosen beim Menschen betrachtetwerden, wurde in dieser Studie der Zusammenhang zwischen dem Vorhandensein von Dermatophyten imHaarkleid von Hunden und Katzen ohne kutane Veränderungen und dem Auftreten der Erkrankung beiden jeweiligen Besitzern untersucht. Insgesamt wurden von Jänner 1999 bis Jänner 2005 Proben von 136Hunden und 248 Katzen genommen. Siebenundachtzig Tiere (22 Hunde und 56 Katzen) gehörten Personen, diean Tinea corporis verursacht durch M. canis, litten und 306 (114 Hunde und 192 Katzen) gehörten Individuenohne Dermatophytose. Alter, Geschlecht, Rasse, Haltung und Jahreszeit wurden für jedes Tier festgehaltenund als mögliche Risikofaktoren untersucht. Dermatophyten wurden bei 20.5% der Hunde und 28.2% derKatzen isoliert. M. canis wurde bei 36.4% der Hunde isoliert, die mit Besitzern lebten, bei denen Tineacorporis diagnostiziert worden war. M. canis wurde aber nie bei Hunden isoliert, deren Besitzer keineHautläsionen zeigten. Im Gegensatz dazu wurde M. canis bei 53.6% der Katzen isoliert, die bei Besitzernmit diagnostizierter Tinea corporis lebten und bei 14.6% der Katzen, deren Besitzer keine Anzeichen derKrankheit aufwiesen. Diese Ergebnisse zeigen deutlich, dass sowohl Katzen als auch Hunde eine bedeutendeQuelle für pathogene Dermatophyten für den Menschen darstellen, auch wenn sie keine klinischenAnzeichen von Dermatophytose aufweisen.© 2006 The Authors. Journal compilation © 2006 European Society of Veterinary Dermatology. 331