VETERINARSKI ARHIV 69 (5), 261-270, 1999

ISSN 1331-8055 Published in Croatia

Epidemiological and clinical features of dermatophytoses in dogs and cats in Croatia between 1990 and 1998

Ljiljana Pinter¹*, Zeljka Jurak¹, Milena Ukalovic²,
and Velimir Sušic³

¹Department of Microbiology and Infectious Diseases,
Faculty of Veterinary Medicine, University of Zagreb, Zagreb, Croatia

²Centre for Reproduction and Animal Breeding of Croatia, Zagreb Croatia

³Department of Animal Breeding and Husbandry,
Faculty of Veterinary Medicine, University of Zagreb, Zagreb, Croatia

* Contact address:
Prof. Dr Ljiljana Pinter,
Department of Microbiology and Infectious Diseases, Faculty of Veterinary Medicine, University of Zagreb, Heinzelova 55, 10000 Zagreb, Croatia,
Fax: 385 1 244 13 90; E-mail: pinter@vef.hr

PINTER, LJ., Z. JURAK, M. UKALOVIC, V. SUŠIC: Epidemiological and clinical features of dermatophytoses in dogs and cats in Croatia between 1990 and 1998. Vet. arhiv 69, 261-270, 1999.

ABSTRACT

Dogs and cats with suspected skin disease referred to the Department of Microbiology and Infectious Diseases, Faculty of Veterinary Medicine, University of Zagreb, over a nine-year period were routinely screened for dermatophyte infections. A total of 5,191 animals (3,353 dogs and 1,838 cats) were examined, from which 1,263 cases of dermatophytoses were detected. The prevalence was found to be higher in cats (P<0.001) than dogs. The species most frequently isolated was Microsporum canis. Infection with Trichophyton mentagrophytes, M. gypseum and M. persicolor was comparatively rare. Infected animals were primarily crossbred dogs and cats, followed by miniature Doberman pinschers, collies, Dalmatians, dachshunds, terriers and boxers in dog, and Siamese and Persians in the cat population. Animals with dermatophyte infection were most often young male animals up to one year of age. The number of cats with clinically evident lesions was significantly higher (P<0.001) when compared to those with no lesion of suspected dermatophyte disease. However, in correlation to dogs there was a significantly higher proportion of irregular alopecia in cats (P<0.001). These results suggest that dermatophytosis, particularly M. canis, is now endemic in Croatia and that this situation is likely to persist. Dermatophytoses will continue to be encountered regularly in our clinical practice.

Key words: dermatophytes, epidemiology, clinical features, dog, cat, Microsporum, Trichophyton, Croatia

Introduction

In Croatia, as in other parts of Europe, ringworm is the zoonosis most likely to be acquired by humans from companion animals (CAPRILLI et al., 1980; ONSBERG and SOLVESTER, 1981; TOROK et al., 1982; LUNDER and LUNDER, 1992; BREUER-STROSBERG, 1993; TERRAGNI et al., 1993; TUREK-URASINSKA, 1993; KORSTANJE et al., 1994). Microsporum canis (M. canis) is now the most common zoophilic species reported from human dermatophytosis in Croatia (KASTELIC and WOLF, 1985; SKERLEV and CAJKOVAC, 1994; TOPOLOVAC et al., 1998). This fungus is found primarily on cats, causes ringworm in a smaller proportion of dogs, and only occasionally infects other species such as rabbits, hamsters or goats (PINTER, 1997).

Until 1982 dermatophyte infections were encountered very rarely in dogs and cats in Croatia. The diseases could usually be traced to imported animals, therefore this part of the Europe was considered free of dermatophyte infections, particularly M. canis (HAJSIG et al., 1975). After 1982 a marked increase of dermatophyte infections with M. canis was observed, which continued until the end of the late eighties (PINTER, 1994).

In the early nineties, during the war period and soon after, a significant increase in diseased animals was noticed in Croatia. The purpose of this study, in the view of this fact, was to identify epidemiological changes concerning dermatophyte diseases in dogs and cats over this period.

Materials and methods

A retrospective study of records during the 9-year period (January 1990 - December 1998), from the Mycology laboratory of the Department of Microbiology and Infectious Diseases at the Faculty of Veterinary Medicine, University of Zagreb in Croatia, was conducted in order to examine the frequency, infecting species, and characteristics of dermatophytoses in dogs and cats.

A total of 5,191 animals (3,353 dogs and 1,838 cats) were examined. The majority of submissions were from animals received at the Faculty of Veterinary Medicine Clinic, but samples with detailed records were also received from field veterinary stations in Croatia. Patient's breed, sex, age and detailed clinical picture with drawn distribution of the lesions, including the results of Wood's lamp examination, were extracted from each medical record. Laboratory data were based on direct microscopy of hair and skin scrapings in lactophenol blue and culture of sampled material on Sabourauds' dextrose agar (Biolife) supplemented with chloramphenicol (0.5 mg/ml) and cycloheximide (0.5 mg/ml). All the specimens were incubated at 27 °C for three to four weeks and suspected dermatophyte cultures were identified by the morphology of the thallus and microscopic appearance of the hyphae, macroconidia and microconidia (REBELL and TAPLIN, 1970). For additional production of macroconidia, isolates were identified also on the basis of characteristic growth on polished white rice or Takashios' medium, where necessary (VANBREUSEGHEM et al., 1978).

Statistics

The data were analysed by using the c² test. A P value of <0.05 was considered significant.

Results

During the 9-year period January 1990 to December 1998, out of 3,353 examined dogs 515 (15.36 %) were found to have dermatophyte infection. A significantly higher proportion (P<0.001) of dermatophyte infections belonged to the M. canis species (468 were M. canis and 47 were other species).

Dog breeds affected by dermatophytes are recorded in Table 1. As can be seen from this table, ringworm was most frequently diagnosed in crossbreeds, which was statistically significant when compared to pure breeds (P<0.001).

Table 1. Relationship between breeds of dog and the prevalence of dermatophytoses in Croatia (only the first 12 with the
highest positive percentage are shown in the table)

Figure 1 presents data on the frequency of positive cases in each year.

Fig. 1. Percentage of dermatophyte positive cats and dogs in Croatia per each year between 1990 and 1998

There was a higher incidence of dermatophytoses in male dogs and animals less than one year old (Table 2). It was also noticeable from history data that ringworm-affected dogs were often in contact with other animals (dogs and cats), even with stray cats. Infections acquired from diseased dogs were recorded in 33 adults and 24 children.

Table 2. Number of positive animals to dermatophytes in Croatia according to sex and age distribution

In Table 3, data concerning clinical observations in dogs with dermatophyte infection are presented. There were too few non-M. canis isolates from dogs to allow statistical comparison, so the majority of data describe the clinical picture of microsporosis. There was a noticeably higher proportion of dogs with suspected clinical lesions to dermatophytosis (P<0.001) than without evident lesions. The frequency of round, sharp-bordered lesions, known as typical ringworm, in correlation to cats was significantly higher (P<0.001) in dogs. Lesions were found most frequently on the head and legs and markedly less frequently in other parts of the body, or all over the body.

Table 3. Distribution of positive dogs to dermatophyte infection
according to clinical appearance in Croatia

In 162 dogs without clinical lesions 32 were not checked by Wood's lamp, and so of the 130 dogs examined 42 were positive under the Wood's light, 69 negative and 19 suspicious or uncertain according to the opinion of the attending clinicians.

Out of 1,838 examined cats 748 (40.7 %) proved to have dermatophyte infection. A significantly higher proportion (P<0.001) of dermatophyte infections belonged to the M. canis species (738). Fig. 1 presents data on the frequency of positive cases in each year.

The most frequently infected animals were crossbred cats (525) followed by either Siamese (15) or various longhaired cats, primarily of Persian species (127).

Further details on clinical manifestation in infected cats from the period 1990 until the end of 1998 are presented in Table 4. The number of cats with clinically evident lesions was significantly higher (P<0.001) when compared to those with no suspect lesions to dermatophyte disease. In correlation to dogs, however, there was a significantly higher proportion of irregular alopecia in cats (P<0.001).

Table 4. Distribution of positive cats to dermatophyte infection
according to clinical appearance in Croatia

Cats with dermatophyte infection were most often young male animals up to one year of age (Table 2). The infected cats were also often in contact with other animals, but this time mostly with other cats (domesticated or stray). By handling or looking after either domesticated or stray cats with dermatophytosis 234 persons contracted the disease, 98 of whom were children.

Discussion

Our findings clearly indicate that ringworm is a serious and important form of skin disease among domestic carnivorous animals. Strong evidence that the highest proportion of dermatophytosis is caused by M. canis was reported, being established in 1,206 (23.23 %) out of 5,191 dogs and cats examined. Other species were isolated, for example: T. mentagrophytes, M. gypseum and M. persicolor, but in far smaller numbers. These findings contrast with those from the United Kingdom, where M. canis together with T. mentagrophytes were the two most common species (SPARKS et al., 1993), or with those from the USA in which M. canis, T. mentagrophytes and M. gypseum comprised together 99 per cent of all canine and feline infections (BLAKEMORE, 1974).

Here again, it was confirmed that infections are more frequent in cats than in dogs (THOMSETT, 1986; WRIGHT, 1989; BREUER-STROSBERG, 1993; SPARKES et al., 1993). Also of interest is the observation that among cats, shorthaired animals are more susceptible to infection that are longhaired, in which ringworm is usually localised at shorthaired covered skin sites (head, legs). However, it is possible that longhaired cats are more often un-diagnosed carriers, as in longhaired animals lesions are sometimes hardly visible. Unfortunately, there were insufficient data to confirm statistically if longhaired cats are significantly more often carriers of dermatophytes, because many of these cases were revealed only after transmission to humans.

The incidence of dermatophyte infections in male dogs and cats appeared higher than in females, but the nature of the population sample could have influenced these findings. Whereas the different prevalence of dermatophytoses in different age groups can be explained by the greater susceptibility of younger animals due to their naive immunological status, closer and more frequent contact with an infected mother and bad zoohygienic conditions for stray kittens.

Also, our observation that among dogs and cats with dermatophyte infections there were more in which skin changes could be visualised than was previously reported, may be primarily the result of selective referral by clinicians and/or owners to our clinic. From the history data it was clear that the owner's decision to check the animals, or the clinicians referral for thorough dermatological examination, depend in almost every case on a suspect lesion. This finding does not support the findings of other authors who identify a higher proportion of dermatophyte cases in the absence of evident lesions (THOMSETT, 1986). This leads us to suspect that there are more undetected dermatophyte infections in our carnivores which should be identified by other indicators, e.g. epidemiological situation, non-cured underlying diseases, complication of primary diseases such as various allergies, atopies, or hormonal disturbances.

Because the clinical signs of ringworm were so variable in both animal species and often so inconspicuous, a laboratory examination was essential to demonstrate infection as well as to identify the dermatophyte responsible. This included examination by Wood's light, which proved to be a more reliable diagnostic method in cats than dogs. One of the reasons for this might be that local treatment begun by the owners of dogs complicated the diagnostic process and, in longhaired dogs particularly, the examination is less precise.

The absence of necessary knowledge on clinical changes in cats, particularly stray kittens, may account for the fact that cats were a more frequent source of human infection. Our findings support this assumption. Also, we believe - as do some other authors - that cats actively carrying M. canis yet showing minimal signs of disease are the reservoirs that maintain and disseminate this infection (BIBERSTEIN, 1990; FOIL, 1990; SCOTT et al., 1995). M. canis does not easily maintain itself saprophytically in the environment, so it is likely that stray cats in big colonies, such as in urban areas, and carrier cats in a breeding establishment, can maintain a cycle of infection passing directly from one animal to another. Unfortunately, clinical examination as currently used at animal shows fails to detect these carriers or to identify breeding colonies where infection exists. The diagnosis of dermatophytosis in adopted stray cats is usually too late, not only for the animal but also for the owner.

Finally, the results presented strongly suggest that the epidemiological situation concerning dermatophytoses, particularly ringworm caused by M. canis, in Croatia has markedly changed. It may be asserted that dermatophytoses in domestic carnivorous animals in this region has already become common, that it is likely to persist, and that we will continue encountering it regularly in our clinical practice.

Acknowledgements
We would like to thank Dr. Richard Anthony for his critical reading as well as all colleagues who participated in clinical work.

References

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Received: 4 October 1999
Accepted: 21 October 1999

PINTER, LJ., Z. JURAK, M. UKALOVIC, V. SUŠIC: Epizootiološke i klinicke osobitosti dermatofitoza u pasa i macaka u Hrvatskoj izmedu 1990. i 1998. Vet. arhiv 69, 261-270, 1999.

SAZETAK

U razdoblju od 1990. do 1998. u mikološkom laboratoriju Zavoda za mikrobiologiju i zarazne bolesti Veterinarskog fakulteta Sveucilišta u Zagrebu pretrazeni su na dermatofite materijali od 5.191 psa i macke. Vecina materijala uzeta je na Klinici Zavoda, a manjim dijelom u veterinarskim ambulantama na podrucju Hrvatske, i poslana na pretragu zbog postavljanja etiološke dijagnoze utvrdene kozne bolesti. Infekcija dermatofitima ustanovljena je u 515 (15,36%) od ukupno 3.353 pretrazena psa i u 748 (40,7%) od ukupno 1.838 pretrazenih macaka. Vecina zivotinja bila je inficirana vrstom Microsporum canis, rjede vrstama Trichophyton mentagrophytes, M. gypseum i M. persicolor. Uz prikaz mikoloških nalaza u radu se raspravlja o epizootiološkim podacima i klinickim nalazima u vezi s pojavom dermatofitoza u domacih mesojeda u Hrvatskoj.

Kljucne rijeci: dermatofiti, epizootiologija, klinicke osobitosti, pas, macka, Microsporum, Trichophyton, Hrvatska