Dermatophytosis, “ringworm”

 

Edited January, 2017

The dermatophytosis guidelines were first published in the J Feline Med Surg 2013, 15: 598-604 by Tadeusz Frymus et al. The present guidelines were updated by Tadeusz Frymus.

 

Synopsis

 

  • Dermatophytosis, caused usually by Microsporum canis, is the most common fungal infection in cats and one of the most important infectious skin diseases in this species.
  • M. canis produces arthrospores that may remain infective for about a year and are easily transmitted by direct contact or by fomites to cats, other animal species and humans.
  • Many cats are infected subclinically or are fomite carriers of the arthrospores.
  • Dermatophytosis may be endemic in groups of cats, especially in a poor environment, and its eradication is difficult in such cases.
  • Circular alopecia, desquamation and sometimes an erythematous margin around central healing (“ringworm”) are typical lesions of this chronic skin disease.
  • In many cats the disease is self-limiting, with only hair loss and scaling. In young animals and immunosuppressed adults, the outcome may be a multifocal or generalised skin disease.
  • The gold standard for the detection of dermatophytes is culture on Sabouraud agar. Wood’s lamp examination and microscopic detection of arthrospores on hairs are much less sensitive.
  • In severe cases systemic and topical therapy must be combined and maintained for several weeks. In catteries and shelters, medication must be accompanied by intensive decontamination of the environment.
  • For systemic therapy itraconazole is the drug of choice.
  • Recommended topical treatment is repeated body rinse with an enilconazole solution or miconazole with or without chlorhexidine.
  • Safe and efficient vaccines for cats against this fungal infection are unavailable; the ABCD does not recommend vaccination.

 

 

Agent properties

 

In contrast to single-celled yeasts, dermatophytes (literally: “skin plants”) are complex fungi growing as hyphae and forming a mycelium (Fig. 1). About 40 species belonging to the genera Microsporum, Trichophyton and Epidermophyton are considered as dermatophytes. Over 90% of feline dermatophytosis cases worldwide are caused by Microsporum canis (Moriello and DeBoer, 2012). Others are caused by M. gypseum, T. mentagrophytes, T. quinckeanum, T. verrucosum or other agents. With the exception of M. gypseum, all of these fungi produce proteolytic and keratolytic enzymes that enable them to utilise keratin as the sole source of nutrition after colonisation of the dead, keratinised portion of epidermal tissue (mostly stratum corneum and hairs, sometimes nails).

 

diagnosis micro

Fig. 1. Microscopic appearance of dermatophytic infection

 

Dermatophytes produce arthrospores, which are highly resistant, surviving in a dry environment for 12 months or more (Sparkes et al., 1994b [EBM grade III]). In a humid environment, however, arthrospores are short-lived. High temperatures (100°C) destroy them quickly. Arthrospores adhere very strongly to keratin.

Depending on the source of infection and reservoirs, dermatophyte species are classified into zoophilic, sylvatic, geophilic and anthropophilic fungi.

 

 

Epidemiology

 

Dermatophytosis is worldwide the most common fungal infection of cats and one of the most important infectious skin diseases in this species. It may be transmitted to other animal species, and is also an important zoonosis (Figs. 2, 3).

 

human nail

Fig. 2 Dermatophytosis on a human nail. Courtesy Andy Sparkes, AHT

human head

Fig. 3 Dermatophytosis on a human head. Courtesy Andy Sparkes, AHT

M. canis is a typical zoophilic dermatophyte. It was generally thought that subclinical infections are very common in cats, especially in longhaired animals over 2 years of age. However, in many groups the prevalence is relatively low. Therefore, M. canis should not be considered part of the normal fungal flora of cats and its isolation from a healthy animal indicates either subclinical infection or fomite carriage (Moriello and DeBoer, 2012).

Arthrospores are transmitted mainly through direct contact with sick or subclinically infected cats, but also dogs or other species (Moriello, 2014). In sick animals, the infected hair shafts are fragile and hair fragments containing arthrospores are very efficient in spreading infection. In addition, uninfected cats can passively transport arthrospores on their hair, thereby acting as fomites. Risk factors include: introducing new animals into a cattery, cat shows, catteries, shelters, mating etc. Arthrospores are easily spread on dust particles, also to rooms without access for cats. Therefore, indirect contact should be considered too (via contaminated collars, brushes, toys, environments etc), though is hardly documented (Moriello, 2014).

 

Outdoor cats, especially in rural areas, can be exposed by digging to M. gypseum, a geophilic fungus living in soil. Cats may be infected with T. mentagrophytes or T. quinckeanum through contact with small rodents, and with T. verrucosum through contact with cattle.

 

 

Pathogenesis

 

Healthy skin acts as an effective barrier against fungal invasion. The increased rate of regeneration of epidermal cells in response to the dermatophyte with the consequent removal of fungus from the skin surface is another protective mechanism. As dermatophytes cannot penetrate healthy skin, many cats are merely passive carriers of the arthrospores or remain subclinically infected. Whether such an infection will lead to clinical disease depends on many factors. Predisposing factors to disease include: a young age (first 2 years of life), immunosuppression (including immunosuppressive treatment), other diseases, nutritional deficits (especially proteins and vitamin A), high temperature and high humidity (Moriello and DeBoer, 2012). Very important for the facilitation of infection is any kind of skin trauma resulting from increased moisture, injury by ectoparasites or scratches due to pruritus, playing or aggressive behaviour, clipping etc. In general, poor hygiene is a predisposing factor. In overcrowded feline groups, social stress may play an important role. This can make eradication of ringworm very difficult in catteries or shelters infected with M. canis.

The potential immunosuppressive effect of feline immunodeficiency virus (FIV) and feline leukaemia virus (FeLV) on the prevalence of fungal infection has been investigated. The higher prevalence of M. canis in FIV-infected animals compared with normal cats reported in one survey (Mancianti et al., 1992) was not observed by another group (Sierra et al., 2000). It has been suggested that any association may be related to differences in the environment rather than to the retroviral status of the cats (Mignon and Losson, 1997).

The incubation period of ringworm caused by M. canis is 1 to 3 weeks. During this time, hyphae grow along the hair shafts through the stratum corneum to the follicles where they produce spores that form a thick layer around the hair shafts. As dermatophytes are susceptible to high temperatures, they cannot colonise deeper parts of the skin or the follicle itself. Therefore, the hair grows normally but breaks easily near the skin surface resulting in hair loss. Several metabolic products of the fungus may induce an inflammatory response in the skin, and may be observed mainly around the infected area forming sometimes ring-like lesions with central areas of healing and papules on the periphery (“ringworm”).

In many immunocompetent cats living in hygienic conditions these lesions are limited (e.g. to the head) and disappear after several weeks. In immunosuppressed animals, the outcome may be a multifocal or generalised skin disease with secondary bacterial infections. On rare occasions, a marked inflammatory reaction to hyphae induces a nodular granulomatous reaction involving dermis and draining on the skin surface. These so-called pseudomycetomas are more often seen in Persian cats, sometimes concurrently with classical lesions.

The pathogenesis of other dermatophyte infections is similar to that described above.

 

 

Immunity

 

Naturally-occurring ringworm is rarely recurrent, suggesting an effective and long-lasting immunity. Experimental studies confirm that animals express increased resistance to subsequent challenge by the homologous fungus. Re-infections may occur, but require a much greater number of spores, and usually these subsequent infections are cleared more rapidly (Moriello and DeBoer, 2012). It has been suggested that for the development of full immunity, the infection must run its entire natural course, as in cats whose infection was aborted with antifungal treatment the delayed type hypersensitivity reactions were often weaker (Moriello et al., 2003).

Although dermatophyte infection is confined to the superficial keratinised tissues, humoral and cellular immune responses are induced. Prominent activation of T helper type 2 (Th2) cells and the corresponding cytokine profile lead to antibody formation followed by chronic disease whereas activation of Th1 cells stimulates a cell-mediated response characterised by interferon-γ, interleukins 12 and 2, and leads to recovery (Sparkes et al., 1995, Moriello and DeBoer, 2012). Such cats are protected against re-infection (Sparkes et al., 1993a). The role of the humoral response in dermatophytosis is unclear, although antibodies could have a fungistatic effect by means of opsonization and complement activation (Sparkes et al., 1994a).

 

 

Clinical signs

 

In many cats, dermatophytes cause a mild, self-limiting infection with hair loss and scaling.

The typical presentation of ringworm in cats is regular and circular alopecia, with hair breakage, desquamation and sometimes an erythematous margin and central healing (Chermette et al., 2008, Moriello and DeBoer, 2012). The lesions are sometimes very small, but occasionally may have a diameter of 4-6 cm. Lesions may be single or multiple, and are localised mostly on the head (Fig. 4), but also on any part of the body, including the distal parts of the legs and the tail. Young cats in particular display lesions localised at first to the bridge of the nose and then extending to the temples, the external side of the pinnae and auricular margins (Fig. 5). Multiple lesions may coalesce. Pruritus is variable, generally mild to moderate and usually no fever or loss of appetite is observed (Chermette et al., 2008, Moriello and DeBoer, 2012).

 

13 Dermatophytosis Fig. 3

Fig. 4. Dermatophytosis lesions start on the head in many cases. Courtesy of International Cat Care (formerly Feline Advisory Bureau)

cat nose

Fig. 5. Lesions on the nose; courtesy Andy Sparkes, AHT

 

In some cats, dermatophytosis can present as a papulo-crustous dermatitis (“miliary dermatitis”) affecting mainly the dorsal trunk.

In immunosuppressed cats, extensive lesions with secondary bacterial involvement are sometimes associated with chronic ringworm. Such patients demonstrate atypical, large alopecic areas, erythema, pruritus, exudation and crusts (Fig. 6). At this stage, dermatophytosis may mimic other dermatological conditions. Typical signs may be still visible at the margins of the lesions.

 

13 Dermatophytosis Fig. 5

Fig. 6. Particularly in immunocompromised cats, dermatophytosis may be multifocal and even generalised. Courtesy of International Cat Care (formerly Feline Advisory Bureau)

 

A rare outcome is onyxis and perionyxis, and exceptionally nodular granulomatous dermatitis (pseudomycetoma) with single or multiple cutaneous nodules, firm and not painful at palpation (Nuttall et al., 2008). Fistulisation of these nodules is possible. Pseudomycetoma occurring as an abdominal mass may be a rare complication of laparotomy in animals with cutaneous dermatophytosis (Black et al., 2001).

 

 

Diagnosis

 

As dermatophytes can produce lesions similar to many feline skin diseases, they should be considered in all cats with any cutaneous disease. If possible, dermatophyte diagnosis should be undertaken before any treatment.

 

Wood's lamp cat

Fig. 7. Preliminary diagnosis: fluorescence under Wood’s lamp illumination. Courtesy Any Sparkes, AHT

 

An inexpensive and simple screening tool for M. canis infection is the Wood’s lamp examination (Figs. 7, 8). During this procedure infected hair shafts show apple-green fluorescence. It is generally believed that this method is not very sensitive as only about 50% of M. canis strains fluoresce and other dermatophytes do not at all (Sparkes et al., 1994c).  Furthermore, debris, scale, lint and topical medications (e.g. tetracycline) can produce false positive results. Thus, Wood’s lamp findings should be confirmed by other methods. However, according to recent finding of Moriello (Moriello, 2014) at least a part of the so called “non-fluorescing strains” might be cultured from cats that were in fact not infected but only passive carriers of spores (and spores do not fluoresce). Similarly, according to her experience a proper examination technique may significantly reduce the number of false positive and false negative results. She also presumed that the discrepancies about the usefulness of the Wood’s lamp may partially result from a different quality of the models available and concluded that a lamp with a central area that allows for magnification of the examined site used by a trained observer is a very useful first-line diagnostic test [EBM grade IV]. Many tips for properly using a Wood’s lamp are included in this review (Moriello, 2014).

 

Wood's lamp paw

Fig. 8. Fluorescence under Wood’s lamp illumination. Courtesy Any Sparkes, AHT

 

Direct microscopic examination is another simple and rapid method to detect dermatophytes on hairs or scales. It is strongly recommended to pluck hairs for this purpose under Wood’s lamp illumination, what is much better than obtaining them from the edge of a lesion (Moriello, 2014). The sample should be cleared with 10-20% KOH before examination, though a direct observation in a drop of mineral oil is possible (Moriello, 2014). There are a number of techniques to improve the visualisation of fungal elements on the hair shafts (Moriello and DeBoer, 2012). Hairs or hair fragments with hyphae and arthrospores are thicker, with a rough and irregular surface. However, direct microscopic examination may give false positive results, especially if saprophytic fungal spores are present or debris is interpreted as fungal elements. Also, the sensitivity of this technique is relative poor and has been assessed as 59% (Sparkes et al., 1993b). Higher sensitivity (76%) has been achieved by fluorescence microscopy with calcafluor white – a special fluorescent stain that binds strongly to structures containing cellulose and chitin (Sparkes et al., 1994c).

Culture on Sabouraud dextrose agar or other media is the gold standard for the detection of dermatophytes. This method is very sensitive and can determine the species. Samples (hairs, scales) should be collected from the margin of new lesions after gently swabbing with alcohol to reduce contamination. If a subclinical infection or passive carriage is suspected, brushing for 5 minutes with a sterile brush is the best method for collecting sample material. A brand-new toothbrush is mycologically sterile (Moriello and DeBoer, 2012). After such procedure, the number of colonies on the plate reflects the severity of the infection and a “pathogen score” system has been adopted by some shelters for treatment monitoring (Moriello, 2014). Several in-office dermatophyte test media (DTM) based on colour change are available commercially. However, few attempts have been made to evaluate the performance of such media with veterinary samples (Chermette et al., 2008). Therefore suspect colonies must be examined microscopically to confirm presence of a fungus (Moriello and DeBoer, 2012).

PCR has been proposed for the detection of M. canis sequences in suspected material from animals (Nardoni et al., 2007).

 

 

Disease management

 

In immunocompetent cats isolated lesions disappear spontaneously after 1-3 months and may not require medication. However, treatment of such cases will reduce the disease course as well as the risk for other animals and humans and contamination of the environment.

Topical therapy is a necessary part of management because it is the only way to kill spores on the hair coat (Moriello, 2014). However, as a treatment it is generally less effective in cats compared to humans due to poor penetration of the medicines through the hair coat, lack of tolerance of this procedure by many cats and the possible existence of unnoticed small lesions. Thus, therapeutic measures should include a combination of systemic and topical treatment, maintained for at least 10 weeks. Generally, cats should be treated not only until the lesions completely disappear, but until the dermatophyte can no longer be cultured from the hairs on at least 2 sequential brushings 1-3 weeks apart.

In catteries and shelters, dermatophyte infection is very difficult to eradicate and is time-consuming and expensive. Good compliance with the owner is therefore essential. A treatment program is necessary, together with complete separation of infected and uninfected animals and intensive cleaning and decontamination of the environment. This will necessitate interruption of breeding programs and shows. It is reasonable to group cats into 3 categories:

  • sick animals (both lesional and culture positive, usually Wood’s lamp positive)
  • subclinically infected (lesion-free, culture positive, usually Wood’s lamp positive)
  • fomite carrier cats (lesion-free, Wood’s lamp negative and negative on repeat fungal culture)

All animals in the cattery should be treated, however the fomite carriers topically only, what avoids long-term expensive and unnecessary systemic therapy.  Special hygiene measures should be taken when handling infected animals in order to prevent infection of humans (gloves, disinfection of cat scratches or any other injury). Many advises for management of infected cat groups have been published recently (Moriello, 2014).

 

 

Topical therapy

 

In cats with a limited number of lesions, hairs should be clipped away from the periphery of lesions including a wide margin. Clipping should be gentle to avoid spreading the infection due to microtrauma. Spot treatment of lesions may be of limited efficacy; instead, whole-body shampooing, dipping or rinsing is recommended. In patients with generalised disease, longhaired cats and for cattery decontamination, clipping the entire cat is useful to make topical therapy application easier and to allow for better penetration of the drug. This approach limits also the spread of the spores into the environment, to people and to other animals. The entire hair coat, including whiskers, should be gently clipped and all infected hairs should be wrapped and disinfected before disposal. Chemical or heat sterilisation of instruments is essential. Cats should not be clipped in veterinary clinics to avoid environmental contamination. The best place for clipping is in the cat’s own household, where the environment is already contaminated.

Topical antifungal drugs differ widely in their efficacy. One of the most effective procedures is a whole body treatment with a 0.2% enilconazole solution performed twice weekly (Moriello and DeBoer, 2012). Local or general side effects are very seldom reported provided that grooming is prevented (Elizabethan collar) until the cat is dry (Hnilica and Medleau, 2002). Very effective is also 2% miconazole with or without 2% chlorhexidine as a twice weekly body rinse or shampoo (Moriello and DeBoer, 2012). In the USA, lime-sulphur solution is commonly used.

 

 

Systemic therapy

 

Itraconazole

Though relatively expensive, itraconazole is currently the preferred drug in feline dermatophytosis and is licensed for this indication (Moriello and DeBoer, 2012). It is comparable (or superior) in efficacy to ketoconazole or griseofulvin and is much better tolerated by cats. The only adverse reaction occasionally reported is anorexia. The embryotoxicity and teratogenicity of itraconazole also seem to be lower than those of ketoconazole. Nevertheless, its administration in pregnancy is not recommended. Use in kittens as young as 6 weeks is possible. Most veterinary dermatologists will use itraconazole as so-called pulse therapy, which is also suggested by the manufacturer. This protocol is effective and also reduces the cost of treatment. A pulse administration of 5 mg/kg/day for one week, every two weeks for 6 weeks has been suggested (Colombo et al., 2001). Another study demonstrated that there were sufficient levels of itraconazole in the plasma and the fur of cats with ringworm that had been given three cycles of treatment consisting of one week with treatment (5 mg/kg) and one week without. A 25-30% reduction in levels was observed after the week without treatment, but the concentrations were still high enough even two weeks after the last administration (Vlaminck and Engelen, 2004 [EBM grade IV]). These data illustrate that such a treatment schedule (3 x 7 days of dosing) provides actual coverage of at least 7 weeks.

 

Terbinafine

An alternative is terbinafine administered orally 30-40 mg/kg once daily (Nuttall et al., 2008, Moriello and DeBoer, 2012). It seems also suitable for pulse therapy. After administration lasting 14 days terbinafine persisted in hair of cats at inhibitory concentrations for 5.3 weeks (Foust et al., 2007 [EBM grade III]). Occasional vomiting and intensive facial pruritus have been observed as side effects.

 

Ketoconazole

Ketoconazole has been used orally 2.5–5 mg/kg twice daily. However, cats are relatively susceptible to side effects with this drug which include liver toxicity, anorexia, vomiting, diarrhoea, and suppression of steroid hormones synthesis. Ketoconazole is also contraindicated in pregnant animals.

 

Griseofulvin

In some countries, griseofulvin is still used. However, now it is generally not recommended as more safe and effective preparations are available. It is administered orally for at least 4-6 weeks at 25-50 mg/kg once to twice daily. Griseofulvin is poorly soluble in water and micronised formulation as well as administration with fatty meals enhance absorption. Adverse reactions include anorexia, vomiting, diarrhoea, and bone marrow suppression, particularly in Siamese, Himalayan and Abyssinian cats. The use of griseofulvin is contraindicated in kittens younger than 6 weeks of age and in pregnant animals as the compound is teratogenic, particularly during the first weeks of gestation. There are a few reports suggesting that FIV infection predisposes cats to griseofulvin-induced bone marrow suppression. Therefore, cats should be tested for this infection prior to therapy. If griseofulvin is chosen, monthly CBCs should be carried out to detect possible bone marrow suppression.

 

Lufenuron

Lufenuron is a chitin synthesis inhibitor, used for the prevention of flea infestations in dogs and cats. As chitin is also a component of the fungal cell wall, an antifungal activity has been expected. However, studies in cats did not demonstrate an antifungal effect and lufenuron is not recommended for the treatment of dermatophytosis (Moriello and DeBoer, 2012).

 

Other options

In cattle and fur-bearing animals, immunotherapy with anti-dermatophyte vaccines is believed to reduce the lesions and to accelerate their disappearance. Although M. canis vaccines have been marketed for treatment of affected cats, controlled studies demonstrating efficacy of this procedure in cats are hard to find. Results of a placebo-controlled-double-blind study performed on 55 cats with severe dermatophytosis caused by M. canis or T. mentagrophytes have recently been published (Westhoff et al., 2010). An inactivated vaccine containing antigens of M. canis, M. canis var. distortum, M. canis var. obesum, M. gypseum and T. mentagrophytes was given three times intramuscularly to sick animals. A trend of improvement in all cats following therapeutic vaccination has been observed, although this improvement was not significantly different from that in the placebo treated cats.

 

 

Environmental decontamination

 

Thorough vacuuming and mechanical cleaning are essential to remove infective material (no visible hairs should be present), especially in households with one or a few cats where disinfection is impractical and unnecessary. However, in catteries or shelters, disinfection is very important. Most disinfectants labelled as “antifungal” are fungicidal against mycelial forms of the dermatophyte or macroconidia but not against arthrospores. Most efficient against arthrospores are 1:33 lime-sulphur, 0.2% enilconazole, and 1:10 to 1:100 household chlorine bleach (Moriello and DeBoer, 2012). All surfaces should be cleaned with one of these solutions. An enilconazole smoke fumigant formulation is available in many European countries.

Detailed decontamination procedures as well as the management of infected catteries and shelters during treatment are described elsewhere (Carlotti et al., 2009, Moriello and DeBoer, 2012, Moriello, 2014). 

 

 

Vaccination

 

Very few efficacy studies on anti-M. canis vaccines (prophylactic or therapeutic) for cats have been performed and published. Although considerable success has been achieved in prophylactic or therapeutic use of anti-dermatophyte vaccines in cattle and fur-bearing animals, a safe and efficient vaccine for cats is still not available (Chermette et al., 2008, Lund and DeBoer, 2008).

A killed M. canis-cell wall vaccine induced both humoral and cell-mediated immunity in experimental cats; however, these responses did not protect cats against challenge (DeBoer and Moriello, 1994). Similarly, M. canis antigens combined with a live Trichophyton vaccine did not induce protective immunity against a topical challenge with M. canis (DeBoer et al., 2002). A commercial vaccine consisting of killed M. canis components in adjuvant was licensed in the USA for treatment of cats rather than prevention. However, in experimental cats, this vaccine did not prevent the establishment of a challenge infection and also did not provide a more rapid cure of an established infection in vaccinated cats compared to unvaccinated controls (DeBoer et al., 2002). The product was withdrawn from the market. Some other studies to develop dermatophytosis vaccines have recently been reviewed (Lund and DeBoer, 2008).

ABCD does not recommend dermatophytosis vaccination.

 

 

References

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