Dermatophytosis in Small Animals Antonella S

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Review Article SOJ Microbiology & Infectious Diseases Open Access

Dermatophytosis in Small Animals Antonella S. Mattei1*, Márcia A. Beber2 and Isabel M. Madrid3 1University Federal of Rio Grande (FURG), Medical School, RS, Brazil 2Undergraduate Student in Dentistry, Federal University of Pelotas (UFPel), Pelotas, RS, Brazil 3Facuty of Veterinary, Zoonosis Center Control, Federal University of Pelotas (UFPel), Pelotas, RS, Brazil

Received: March 06, 2014; Accepted: September 19, 2014; Published: November 04, 2014

*Corresponding author: Antonella Souza Mattei, University Federal of Rio Grande (FURG), Medical School, RS, Brazil, Tel: +55(53)-91447884; E-mail: an- [email protected]

Originally soil inhabitants, dermatophytes have evolved to Abstract geophilic, zoophilic, and anthropophilic species based on their dermatophytosis in small animals. In the last years, the pet population maininfect habitat animals or andhost. humans Three dermatophytes and are accordingly genera classifiedTrichophyton into, has increasedThe purpose as well of the this interest article in having was animals to briefly as pets. review Because about of Microsporum, and Epidermophyton-comprise more than 40 this, these small animals are more and more inserted in our daily life. different species [4,5]. The understanding of ringworm epidemiology, diagnosis, treatment and control in pets is very important for the reason that pets are often Animals can be infected by a great variety of dermatophytes, asymptomatic carriers of dermatophytes being important sources of mostly zoophilic but also geophilic species, and exceptionally infection and/or carriers of infection. So, it is very important to know about this disease to reduce the spread of zoophilic fungal infections anthropophilic dermatophytes (Table 1) [6]. in humans, considering the close contact between pets and their Clinical importance is usually mild except in heavily infected owners, especially between children and their pets. young animals such as calves with an impact on general health Keywords: Cat; Dog; Exotic pet mammals; Microsporum spp.; condition and growth. On the contrary, serious economic Trichophyton spp.; Zoonosis; Dermatophytosis; Mycosis consequences result from the long duration of the disease [1,6]. The understanding of ringworm epidemiology, diagnosis, Abbreviations treatment and control in pets is very important for reducing the spread of fungal infections in animals and humans. The purpose FeLV: Feline Leukemia Virus; Virus; KOH: Potassium Hydroxide; Min: Minutes FIV: Feline Immunodeficiency small animals. Introduction of this article was to briefly review about dermatophytosis in In recent years, both the number of domestic pets fed Table 1: Zoophilic and Geophilic dermatophytes species in animals. inside their owners’ homes and the interest in having animals Dermatophytes species Main source Others as pets at one’s home have increased markedly. Considering Microsporum canis Cat, dog, horse All mammals the close contact between pets and their owners, especially Microsporum gallinae poultry Dog, cat between children and cats and dogs, these animals that are Microsporum gypseum Soil All mammals often asymptomatic carriers of dermatophytes can be important sources of infection and/or carriers of infection [1]. Microsporumn nanum Soil Pig Microsporum persicolor Microtid rodents Dog, cat However, nowadays not only cats and dogs are popular pets, the exotic companion mammals (e.g. rabbits, rodents, ferrets, Trichophyton equinum Horse Cat, dog (rare) hedge hogs) are also common and they can be a potential source Trichophyton erinacei Hedgehog Dog of zoonotic infections transmissible to their owners [2]. Trichophyton Rodents All mammals mentagrophytes Trichophyton simii Primate Fowl, dog, cat Dermatophytosis is characterized by a superficial skin Cattle, other fungal disease in clinical veterinary medicine in small animals. Trichophyton verrucosum All mammals Theseinfection fungi confined produce to keratinisedkeratinases epithelium,and others isenzymes the most capable common to ruminants digest the keratin protein complex, allowing the dermatophyte Note: Other geophilic species are frequently isolated from hair coat of M. to burrow deeper into the stratum corneum in the host and cookei, M. praecox (frequent in the equine environment and sometimes pathogenicmammals, but, for man),usually, T. without ajelloi, T. pathogenic terrestre. Some significance rare cases in animals: of animal ringworm due to anthropophilic dermatophytes (E. floccosum, T. rubrum therefore to elicit an inflammatory reaction. The,4]. degree of and T. tonsurans in dog; T. violaceum in pig) have been reported. inflammation, dependent of host-fungus interaction, determines the degree and significance of the clinical signs [3 Symbiosis Group *Corresponding author email: [email protected] Dermatophytosis in Small Animals Copyright: © 2014 Mattei et al.

Etiology

three genera, Epidermophyton, Microsporum, and Trichophyton [4,7].The The etiologic descriptions agents of the the dermatophytoses genera are essentially are classified followed in by the colony macroscopic aspects (diameter, texture, surface color and reverse color) and themicroscopic aspects (conidial morphology and formation of conidia). They both are updated following the discovery of new species. The genera and their descriptions are as follows: 1A) 1B)

Epidermophyton spp: The type species is Epidermophyton Figure 1: Microsporum canis culture, macroscopic colony (A) and mi- floccosum croscopic observation in lactophenol (B) (Veterinary Mycology Labora- turning into powder surface, central poor radial grooves and tory, MICVET, Federal University of Pelotas, Rio Grande do Sul, Brazil). white color(Figure turning 1A intoand B). yellow-green The colony oraspects mustard-yellow are filamentous and brown-yellow reverse in Sabouraud dextrose agar at 25°C. The macroconidia are broadly clavate with typically smooth, thin to moderately thick walls and one to nine septa, 20 to 60 by 4 to

clusters. Microconidia are absent. This genus has only two known species13 mm into size.date, They and only are usuallyE. floccosum abundant is pathogenic and borne [7-11]. singly or in Microsporum spp: The type species is Microsporum canis (Figure 2A and B). The colony aspects are plane, velvety or cottony surface, white or yellowish color and brown or golden- 2A) 2B) yellow reverse in Sabouraud dextrose agar at 25°C. Macroconidia are characterized by the presence of rough walls which may be Figure 2: Microsporum gypseum culture, macroscopic colony (A) and asperulate, echinulate, or verrucose. They are fusiform, obovate microscopic observation in lactophenol (B) (Veterinary Mycology Labo- (egg shaped) or cylindrofusiform. They may also have thin, ratory, MICVET, Federal University of Pelotas, Rio Grande do Sul, Bra- zil). moderately thick to thick walls and 1 to 15 septa and range in size from 6 to 160 by 6 to 25 mm. Microconidia are sessile or stalked and clavate and usually arranged singly along the hyphae or in racemes [7-11]. Trichophyton spp: The type species is Trichophyton mentagrophytes var. Mentagrophytes . The colony aspects are plane, white to cream color, powdery to granular surface and reverse yellowish(Figure brown to 3A reddish-brown and B) in Sabouraud dextrose agar at 25°C. Macroconidia, when present, have smooth, usually thin walls and one to 12 septa, are borne singly or in clusters, and may be elongate and pencil shaped, 3A) 3B) clavate, fusiform, or cylindrical. They range in size from 8 to Figure 3: Trichophyton mentagrophytes var. mentagrophytes culture, 86 by 4 to 14 mm. Microconidia, usually more abundant than macroscopic colony (A) and microscopic observation in lactophenol (B) macroconidia, may be globose, pyriform or clavate, or sessile or (Veterinary Mycology Laboratory, MICVET, Federal University of Pelo- stalked, and are borne singly along the sides of the hyphae or in tas, Rio Grande do Sul, Brazil). grape-like clusters [7-11]. In 1999, the Trichophyton tonsurans, T. mentagrophytes There are genotypic and phenotypic variations between isolates of the same species of dermatophyte. The clinical taxa, T. tonsurans, T. interdigitale (anamorph of Arthoderma application of these variations has to be discovered yet. These vanbreuseghemiiand related species), T. mentagrophytes, and varieties were T. simii reclassified (anamorph into of A. 5 simii) and T. erinacei (anamorph of A. benhamiae). In 2007, this was epidemiological data [14]. variations do not reflect differences in symptomatology or chaged by treating T. mentagrophytes as the anamorph of A. simii The fungal pathogenicity factors, such as enzyme production, in place of T. simii and adding another anamorph of A. benhamiae, were associated with different clinical dermatophytosis pictures. Trichophyton spp. Furthermore, in 2010 T. mentagrophytes was Apparently, studies examining the enzyme production through replaced by T. simii and treated again as an individual species, i.e. molecular characterization and expression during infection are T. mentagrophytes var. quinckeanum [12]. an importante means to understand the details of pathogenicity Nowadays, the three genera, Epidermophyton, Microsporum, and may also answer questions related to the different degrees of and Trichophyton, virulence observed in different hosts [14-17]. On the basis of dermatophyte primary habitat associations, can be identified based on molecular taxonomic they are separated into three species: anthropophilic, technique [13].

Citation: : 1-6. DOI: Page 2 of 6

Mattei AS, Beber MA, Madrid IM (2014) Dermatophytosis in Small Animals. SOJ Microbiol Infect Dis 2(3) http://dx.doi.org/10.15226/sojmid/2/3/00124 Dermatophytosis in Small Animals Copyright: © 2014 Mattei et al.

zoophilic, and geophilic. Anthropophilic dermatophytes are dermatophytosis due to Microsporum spp. The most common main related with humans and unusually infect other animals T. mentagrophytes (e.g. Epidermophyton floccosum). Zoophilic dermatophytes whereas Microsporum commonly infect animals or are associated with animals however dermatophyte identified was (53.1%), In Brazil, the study about the occurrence of yeasts and sometimes can infect humans (e.g. Microsporum canis). Geophilic spp. occurred only in 3.7% of the cases [2]. dermatophytes in shearing tools used in pet shops as well as dermatophytes are found on soil together with keratinous human or animal materials (hair, feathers and scales) (e.g. Microsporum 58 samples (n = 150), 58.6% of which from clippers and 41.4% gypseum). These species may cause infection in human and veterinary offices and clinics, the fungal isolation was positive in animals [4, 6-10,18]. Microsporum canis, along with M. gypseum and T. epidemiologicalfrom slickers, resulting data regarding in 78 distribution yeast isolates; of dermatophytes but, filamentous in mentagrophytes var. mentagrophytes, are the fungal species veterinaryfungi from environments the dermatophytes are scare. group were not found [23]. The responsible for more than 95% of all dermatophytosis cases in Transmission of dermatophytic infections between conidia from the environment or from existing hosts and new recipients petsCarriage [3,18]. of M. canis is quite frequent in cats. The animal can occur through direct contact with infected animals or can be asymptomatic though some infected hairs are present. indirectly from contaminated fomites, all circumstances that This mechanical carriage, not associated with infection, will be favour those contacts act as predisposing factors. Conidia are very revealed through fungal cultures [6,19,20]. Whereas, the exotic resistant and may remain viable in the environment for years pet mammals can be asymptomatic carriers of T. mentagrophytes [4,6], this explains why the use of material that is shared between var. mentagrophytes [2]. animals favours the contamination. For geophilic dermatophytes, the soil is the reservoir in which the fungi multiply. Thus, the risk Epidemiology of contamination is higher for animals with outdoor contacts A large variety of species have been isolated from domestic, [6,20,22]. captive and free-living animals, but some of them are more Maraki and Tselentis [24] analyzed 111 cases of human often associated with a particular host. The situation is more dermatophytosis due to M. canis according to the origin of

as saprobes and can become parasites for some of them [6,21]. humans, in 91 cases (82%) the infection transmitted by cats Thediversified prevalence with ofthe dermatophytoses geophilic dermatophytes varies according that multiply to climate, in soil infection; in 15 cases (13.5%) the infection was transmitted by temperature, relative humidity and precipitation in different by dogs. Katoh et al. [25] examined the scalps of patients with geographical regions, as well as the natural reservoirs [20]. dermatophytosisand in only five cases due to(4.5%) M. canis was yetthe withoutinfection scalp was transmitted lesions and In Italy, M. canis is the most common dermatophyte isolated the scalps of their family members without dermatophytoses. from dogs and from tinea capitis and tinea corporis in men. Geophilic dermatophytes species (M. gypseum and T. terrestre) those who lived in homes where cats were kept and in only 25% Dermatophyte fungi were detected in 93.8% of the scalps of have been isolated in dogs with a prevalence ranging from 2.2 of homes without cats. to 8.7% [22]. This variation allegedly occurs due to difference in Animals younger than one year-old appear to be susceptible temperature, climate, relative humidity and precipitation among to dermatophytoses, but there is no apparent sex predisposition the geographical regions where the surveys were executed, along [2,5,26-28]. with the degree of experience of clinicians collecting the samples [20,22]. higher prevalence of dermatophytoses, mainly caused by M. canis The prevalence of dermatophytes in dogs range from 4% to (46.4%),As for than breed, other Yorkshire breeds. Thisterriers could had be a explained statistically by qualitativesignificant

defences, sebum and sweat, rather than by their long hair. 10% and a few studies show a higher prevalence [3,20]. However, These animals can be asymptomatic, with higher percentage and Geophilicand/or quantitative dermatophytic differences species, instead, in non-specific were mainly cutaneous found on in cats, the frequency of positive findings is greater than 20%. carriers of dermatophytes, important sources of infection and/or sheepherders and half-breed dogs probably due to different life carriers of infection [20].Canine dermatoses were investigated in style factors rather than to breed. Persian cats were infected only by M. canis while European and half-breeds were also affected by dogs had dermatophytes represented by M. canis for 6.6% of the geophilic dermatophyte species. The high prevalence of infection Brazil during a 1998–2003 period, and 107 (9.8%) out of 1,089 animals and M. gypseum by M. canis in Persian cats may be explained by the fact that they In the frequency study about exotic pet mammals, are more likely to be kept together in large groups where M. canis for 3.0% [6]. may readily spread. The presence of Geophilic dermatophyte species in European and half-breed cats can be explained by their cases,Dermatophytosis T. mentagrophytes was present in 50% (23/46) guinea pigs, 32.6% (15/46) in rabbits and 8.7% (4/46) in chinchillas. In all environment in contact with the soil [22]. specific life style, namely their tendency to live in the outdoor in which both Microsporum was the only dermatophyteT. mentagrophytes identified. Mere exposure to dermatophyte spores does not guarantee The remaining 8.7% were composed of ferrets [6.5% (3/46)], infection. An unknown but “critical mass” of spores must come spp. (2/3) and (1/3) were identified. And 2.2% (1/46) were rats affected by Citation: : 1-6. DOI: Page of 6

Mattei AS, Beber MA, Madrid IM (2014) Dermatophytosis in Small Animals. SOJ Microbiol Infect Dis 2(3) 3 http://dx.doi.org/10.15226/sojmid/2/3/00124 Dermatophytosis in Small Animals Copyright: © 2014 Mattei et al.

into contact with a susceptible host. The spores must evade of fungal hyphae and/or ectothrix spores. This procedure can be host defence mechanisms that include mechanical removal, done with clearing agents such as Potassium Hydroxide (KOH)

fungistatic properties of epidermal lipids, low humidity of the test were considered predictive in relation to positive cultures, skincompetition surface andwith acquired normal bacterialhost immunity and fungal [29]. flora, exposure to which10 or are 20% considered [9,10,34]. as The the positivitygold standard. values Fungal for the elements KOH direct were observed in 61.0% of the cases analyzed. The sensitivity of this Factors that favour infection include any pre-existing test varied from one fungus to another, with the clinical specimen disease that will cause an increase in surface humidity, cause examined originating from the more sensitive dogs making up a microtrauma to the skin and/or compromise host immune surveillance. Once a nidus of infection has been established, the but false negatives were seen, 5.8% in dogs and 20% in cats. fungal species proceeds to invade the keratin of hairs and skin Thus,total of it 63%, is possible and in to cats conclude 57.1%. thatThere direct were examinations no false positives, could and establish infection. Recovery from infection is dependent be very important in the diagnosis of dermatophytoses, since, upon a competent cell mediated immune response [4,29]. if carried out by experienced professionals, it can certainly aid The concomitance of diseases such as hyperadrenocorticism, veterinarians by shortening the time required to initiate adequate or the use of some treatments, mainly corticotherapy, may favour treatment [29]. appearance and worsening of fungal lesions through impairment

(FIV) and the Feline Leukemia Virus (FeLV) are the potential is considered the “gold standard” for diagnosis. The two most Definitive diagnosis is made by fungal culture. Fungal culture immunosuppressiveof immunity. In cats, effect the for developed Feline Immunodeficiency this mycosis [6,18]. Virus commonly used fungal culture media include Sabouraud’s

Clinical Presentation is a valuable adjunct to direct microscopy and is essential at dextrose agar and dermatophyte test medium [9,10,34]. Culture The general presentation of ringworm in animals is a regular least in all nail infections and in any infection to be treated by and circular alopecia, with erythematous margin and a thin systemic medication. In all cases, a medium selective against desquamation. Pruritus is generally absent although described most nondermatophytic molds and bacteria is used as a in a noticeable proportion of animals in some surveys. Lesions primary isolation medium. Cycloheximide is incorporated can be single or multiple, and are localized on any part of the into this medium as a semiselective agent to reduce the animal although the anterior part of the body and the head seem growth of nondermatophytic fungi. Sabouraud agar amended more frequently involved. Usually, there is a centrifugal spread with cycloheximide and chloramphenicol is commonly used. of lesions. Multiple lesions may coalesce, while a spontaneous Dermatophytoses recently treated with antifungal agents may healing at the center with regrowth of hairs is generally observed [6,18]. molds, usually with revealing inconsistency from specimen to repeatedly show uncultivable filaments and grow spurious Kerion (nodular dermatophytosis) is a round and nodular edematous reaction to dermatophyte infection, with a patch of specimenBiochemical [8-10,34]. test were employed to differentiate Trichophyton erythematous scaling alopecia, characterized by a granulomatous spp. are enriched medias with urea, thiamine, histidine, nicotinic acid and inositol, the isolates are subcultured in this media [11]. it is caused mainly by the species of dermatophytes M. gypseum, Bromocresol purple (BCP)–casein–yeast extract agar for the rapid M.dermatitis canis and to aT. deep mentagrophytes pyogranulomatous inflammation. In animals T. verrucosum in specimens from rural areas, this described a kerion by M. gypseum causing a circular lesion on the medium turns from its sky blue original colour to violet within [18,30,31]. Ferreira et al. [32] identification4-7 days in the of presence of T. mentagrophytes, thus permitting the differentiation with T. rubrum and M. persicolor. In addition, nostrilMycetoma-like in a Dachshund, lesions the have first beencase report reported, in Brazil. mostly in Persian it contains casein which is hydrolysed by T. verrucosum and cats, in which the dermatophyte develops in the dermis and the Trichophyton violaceum var. glabrum. When the isolate secretes subcutis. At examination, single or multiple cutaneous nodules, proteases, a broad zone of clearing is observed in the opaque casein, surrounding the small colonies. The urea agar medium the neck and tail basis are visible. Skin on the nodule is darkened may therefore be useful to differentiate T. rubrum (urease -) withfirm and a blue not or painful violaceous at palpation, color, without usually alopeciasituated oron erythema.the back, from T. mentagrophytes var. interdigitale (urease +). With urease- producing strains, urea is splitted into ammonia, resulting in a pH change to alkaline and therefore in the change of the colour FistulisationDiagnosis of the nodule is possible [6,30,31,33]. of the phenol redcontaining medium from a straw yellow to pink fuchsia after 2 (urea-indole broth) or 6 (Christensen’s agar) days hair shafts of M. canis-infected hairs. Infections by M.canis, Wood’s lamp examination looks for fluorescence on the of incubation at 27°C. Thus, T. verrucosum and T. concentricum require for growth the presence of thiamine and inositol. When this technique, the use and interpretation. This examination is a approximately 50% fluoresence, besides this, several flaws in the vitamin requirement is partial, a reduced growth is observed on control medium and for instance, thiamine stimulates examination and/or culture; a negative test does not rule out Trichophyton tonsurans and T. violaceum. Nutritional test media infectionscreening [18]. tool and it is helpful for identification of hairs for direct are commercially available (Trichophyton agars 1–7, Difco®). Direct examination of hairs and scales looks for the presence Assimilation of sorbitol can also be used to differentiate T. rubrum

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(positive) from T. mentagrophytes There are studies reporting on the use of fungal vaccines in cats to prevent dermatophytosis. A killed dermatophyte vaccine Skin biopsy is helpful in the diagnosis of kerion reactions and (negative) [35]. for treatment of M. canis in cats is available (Fel-O-Vax, Fort granulomatous infections because cultures are often negative, Dodge Laboratories). This product is licensed and used for the but don’t know the species involved. With the advent of molecular treatment and prevention of lesions, but not diseases. In another technology, it has been possible to compare the molecular and study, an experiment was done using a combined live-inactivated dermatophyte vaccine and a killed commercially available dermatophyte vaccine were evaluated for prophylactic immunity conventionalThis diagnosis taxonomy are of based dermatophyte on the species molecular [29,34]. taxonomic technique to identify and compare the isolate species for infection nor provided a more rapid cure when compared with eachand anyother therapeutic or with untreated benefit. control. Neither However, vaccine vaccination prevented was the epidemiologyTreatment studies [13]. associated with a slightly reduced severity of initial infection when compared with controls. Interest in vaccination as a treatment or The therapeutic measures should include the combination of systemic and topical treatment. An appropriate duration of treatment must be respected [18]. prophylaxisConclusion continues to be an area of intense research [29, 38]. Topical treatment with enilconazole, polyene and miconazole Dermatophytoses are the most common infectious skin has consistent antifungal activity. The enilconazole should not diseases detected in small animals, in veterinary clinics. The be rinsed from the hair coat and a contact time of 10 min for knowledge about epidemiology, clinical presentation and diagnosis of ringworm are important for treatment, prevention, chlorhexidine (as a single agent), and povidine iodine have been and control, besides public health problem, as the pet population consistentlymiconazole shampoos ineffective is antifungal recommended agents for when efficacy. tested Captan, using has increased in the last years and these animals are more isolated infective spores and/or hairs and are not recommended inserted in our daily life, maintaining close contact with us, especially with our children. Moreover, we have to consider that with systemic therapy; if cost constraints do not allow for due to the high resistance of dermatophyte arthroconidia. concurrentfor use [18,36]. systemic Topical therapy, therapy twice should weekly be used applications in conjunction of fomites and the environment are the efficient sources of infection Acknowledgement consecutive fungal cultures) are obtained [18]. enilconazole can be used until a mycological cure (2-3 negative The authors thank Veterinary Mycology Laboratory (MICVET) Conventional systemic treatment relies on oral antifungal of Federal University of Pelotas, Rio Grande do Sul, Brazil.

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Mattei AS, Beber MA, Madrid IM (2014) Dermatophytosis in Small Animals. SOJ Microbiol Infect Dis 2(3) http://dx.doi.org/10.15226/sojmid/2/3/00124